Thioredoxin-mediated ROS Homeostasis Explains Natural …€¦ · 29-01-2018 · Original: Mutation of DCC1 or CA2 results in the increased ROS levels. A, s of ROS in calli ofLevel

CORRECTION Original Article Published to Plant Phys Preview on July 19, 2017

Zhang H, Zhang TT, Liu H, Shi DY, Wang M, Bie XM, Li XG, and Zhang XS. Thioredoxin-mediated ROS homeostasis explains natural variation in plant regeneration. The authors have acknowledged that errors were made in the creation of some of the figures for this article. The description of the figure corrections in detail is shown as follows. Both original and corrected figures are provided for ease of comparison. In the original Figure 3, the gel blot images in Figure 3B and 3D were overly contrasted and tightly cropped. The upper image in Figure 3B and images in Figure 3D were combined from two gels, respectively. In the corrected Figure 3, the images of Figure 3B and 3D are appropriately cropped and provided without any manipulations of contrast. Three white lines have been inserted to separate the upper image in Figure 3B and images in Figure 3D, respectively. The legend of the figure has been changed accordingly for clarity. In the original Figure 5, the gel blot image in Figure 5A and 5B was overly contrasted and tightly cropped. In the corrected Figure 5, the images of Figure 5A and 5B are appropriately cropped and provided without any manipulations of contrast. The figure legend has not been changed. In the original figures, the background of plantlet images in Figures 1, 4, 6, 7, 8, and 12 have been cosmetically adjusted/cleaned. In the corrected figures, the plantlet images in Figures 1, 4, 6, 7, 8, and 12 are provided without any manipulations of adjusting/cleaning. The figure legends have not been changed.

Plant Physiology Preview. Published on January 29, 2018, as DOI:10.1104/pp.17.00633

Copyright 2018 by the American Society of Plant Biologists

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CORRECTION

Zhang H, Zhang TT, Liu H, Shi DY, Wang M, Bie XM, Li XG, and Zhang XS. Thioredoxin-mediated ROS homeostasis explains natural variation in plant regeneration. The authors have acknowledged that errors were made in the creation of some of the figures for this article. The description of the figure corrections in detail is shown as follows. Both original and corrected figures are provided for ease of comparison. In the original Figure 3, the gel blot images in Figure 3B and 3D were overly contrasted and tightly cropped. The upper image in Figure 3B and images in Figure 3D were combined from two gels, respectively. In the corrected Figure 3, the images of Figure 3B and 3D are appropriately cropped and provided without any manipulations of contrast. Three white lines have been inserted to separate the upper image in Figure 3B and images in Figure 3D, respectively. The legend of the figure has been changed accordingly for clarity. In the original Figure 5, the gel blot image in Figure 5A and 5B was overly contrasted and tightly cropped. In the corrected Figure 5, the images of Figure 5A and 5B are appropriately cropped and provided without any manipulations of contrast. The figure legend has not been changed. In the original figures, the background of plantlet images in Figures 1, 4, 6, 7, 8, and 12 have been cosmetically adjusted/cleaned. In the corrected figures, the plantlet images in Figures 1, 4, 6, 7, 8, and 12 are provided without any manipulations of adjusting/cleaning. The figure legends have not been changed.



Figure 3. Original: DCC1 interacts with CA2. B, Interaction between DCC1 and CA2 in pull-down assay. GST-pull-down protein was detected by immunoblotting using anti-His antibody. D, Interaction between DCC1 and CA2 in co-immunoprecipitation assays. Immunoprecipitated protein with anti-GFP was detected by immunoblotting using an anti-MYC antibody.

Figure 3. Corrected: DCC1 interacts with CA2. B, Interaction between DCC1 and CA2 in pull-down assay. 10% Input and GST-pull-down proteins were detected by immunoblotting using anti-His antibody, respectively (upper gels). CA2-GST and GST proteins were detected by immunoblotting using anti-GST antibody (lower gel). D, Interaction between DCC1 and CA2 in co-immunoprecipitation assays. 10% Input and immunoprecipitated proteins with anti-GFP were detected by immunoblotting using an anti-MYC antibody, respectively (upper gels). 10% Input and



DCC1-GFP proteins were detected by immunoblotting using an anti-GFP antibody, respectively (lower gels).

Figure 5. Original: DCC1 regulates complex I activity via CA2 protein. A and B, CA2 dimmer and oligomer were reduced by DCC1. Purified CA2-His protein was incubated in the assay mixture with or without DCC1 GST-cleaved protein (5 μM) for 30 min at room temperature and then subjected to nonreducing (A) or reducing (B) SDS-PAGE followed by immunoblot analysis. DTT (0.3 mM) was added to recycle DCC1 Trx activity. The position of the monomer, dimmer and oligomer of CA2 are indicated. CA2 dimmer and oligomer showed significantly reduced levels when incubated with DCC1 proteins (right lane). The reaction mixture without DCC1 proteins was used as the control (left and middle lanes).

Figure 5. Corrected: DCC1 regulates complex I activity via CA2 protein. A and B, CA2 dimmer and oligomer were reduced by DCC1. Purified CA2-His protein was incubated in the assay mixture with or without DCC1 GST-cleaved protein (5 μM) for 30 min at room temperature and then subjected to nonreducing (A) or reducing (B) SDS-PAGE followed by immunoblot analysis. DTT (0.3 mM) was added to recycle DCC1 Trx activity. The position of the monomer, dimmer and oligomer of CA2 are indicated. CA2 dimmer and oligomer showed significantly reduced levels when incubated with DCC1 proteins (right lane). The reaction mixture without DCC1 proteins was used as the control (left and middle lanes).



Figure 1. Original: Shoot regeneration is inhibited in dcc1 mutant. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B), and number of shoots per callus (C) in wild type (Col-0), dcc1, and dcc1 ProDCC1:DCC1 cultured on SIM at indicated times.

Figure 1. Corrected: Shoot regeneration is inhibited in dcc1 mutant. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B), and number of shoots per callus (C) in wild type (Col-0), dcc1, and dcc1 ProDCC1:DCC1 cultured on SIM at indicated times.



Figure 4. Original: Loss-of-function of CA2 caused the decreased capacity of shoot regeneration. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B) and number of shoots per callus (C) in wild type (Col-0), ca2, and ca2 ProCA2:CA2 cultured on SIM at indicated times.

Figure 4. Corrected: Loss-of-function of CA2 caused the decreased capacity of shoot regeneration. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B) and number of shoots per callus (C) in wild type (Col-0), ca2, and ca2 ProCA2:CA2 cultured on SIM at indicated times.



Figure 6. Original: Mutation of DCC1 or CA2 results in the increased ROS levels. A, Levels of ROS in calli of Col-0, dcc1, ca2, and dcc1ca2 on CIM and SIM at indicated times by DAB staining.

Figure 6. Corrected: Mutation of DCC1 or CA2 results in the increased ROS levels. A, Levels of ROS in calli of Col-0, dcc1, ca2, and dcc1ca2 on CIM and SIM at indicated times by DAB staining.



Figure 7. Original: Treatment with exogenous ROS inhibits shoot regeneration. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B) and number of shoots per callus (C) in wild type (Col-0) after treatment with H2O2 at different concentrations during shoot regeneration.

Figure 7. Corrected: Treatment with exogenous ROS inhibits shoot regeneration. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B) and number of shoots per callus (C) in wild type (Col-0) after treatment with H2O2 at different concentrations during shoot regeneration.



Figure 8. Original: Decreased ROS level rescues phenotypes of dcc1ca2 double mutant. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B), and number of shoots per callus (C) in wild type (Col-0), dcc1, ca2, and dcc1ca2 after treatment with GSH (600 μM) or overexpression of CAT3 on SIM at 28 days. Glutathione (GSH) is a main endogenous antioxidant responsible for ROS removal. CAT3 encodes a catalase, which catalyzes the breakdown of H2O2 into water and oxygen, thereby reducing the H2O2 level. pER8-CAT3 represents the over-expression of CAT3 in dcc1, ca2, and dcc1ca2 background when induced with estradiol, respectively.



Figure 8. Corrected: Decreased ROS level rescues phenotypes of dcc1ca2 double mutant. A to C, Callus morphology (A), frequencies of shoot regeneration from calli (B), and number of shoots per callus (C) in wild type (Col-0), dcc1, ca2, and dcc1ca2 after treatment with GSH (600 μM) or overexpression of CAT3 on SIM at 28 days. Glutathione (GSH) is a main endogenous antioxidant responsible for ROS removal. CAT3 encodes a catalase, which catalyzes the breakdown of H2O2 into water and oxygen, thereby reducing the H2O2 level. pER8-CAT3 represents the over-expression of CAT3 in dcc1, ca2, and dcc1ca2 background when induced with estradiol, respectively.



Figure 12. Original: ROS levels are associated with shoot regeneration capacity of different ecotypes in Arabidopsis. A, DAB staining showing ROS levels in calli of different ecotypes of Hap1 cultured on SIM at 16 days. B, DAB staining showing ROS levels in calli of different ecotypes of Hap2 cultured on SIM at 16 days.

Figure 12. Corrected: ROS levels are associated with shoot regeneration capacity of different ecotypes in Arabidopsis. A, DAB staining showing ROS levels in calli of different ecotypes of Hap1 cultured on SIM at 16 days. B, DAB staining showing ROS levels in calli of different ecotypes of Hap2 cultured on SIM at 16 days.



1

Thioredoxin-mediated ROS Homeostasis Explains Natural Variation in 1

Plant Regeneration 2

Hui Zhang2, Ting Ting Zhang2, Hui Liu2, De Ying Shi, Meng Wang, Xiao Min Bie, Xing Guo Li*, 3

and Xian Sheng Zhang* 4

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State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, 6

Tai’an, 271018, China 7

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1The work was supported by the National Natural Science Foundation of China (31270231, 9

91217308). 10

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2 These authors contributed equally to this work. 12

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* Address correspondence to [email protected] and [email protected]. 14

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X.S.Z., X.G.L. and H.Z. conceived and designed the experiments; H.Z., T.T.Z., H.L., D.Y.S., M.W. 16

and X.M.B. performed the experiments; X.S.Z. and X.G.L. analyzed data and wrote the article. 17

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Short title: Regulation of Thioredoxin in Plant Regeneration 19

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One sentence summary: Thioredoxin-dependent redox modification regulates plant regeneration 21

via modulation of ROS homeostasis. 22

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Plant regeneration is fundamental to basic research and agricultural applications. The regeneration 29

capacity of plants varies largely in different genotypes, but the reason for this variation remains 30

elusive. Here, we identified a novel thioredoxin DCC1 in determining the capacity of shoot 31

regeneration among Arabidopsis natural variation. Loss-of-function of DCC1 resulted in inhibited 32

shoot regeneration. DCC1 was mainly expressed in the inner tissues of the callus and encoded a 33

functional thioredoxin that was localized in the mitochondria. DCC1 protein directly interacted with 34

CARBONIC ANHYDRASE 2 (CA2), which is an essential subunit of respiratory chain NADH 35

dehydrogenase complex (Complex I). DCC1 regulated Complex I activity via redox modification of 36

CA2 protein. Mutation of DCC1 or CA2 led to reduced Complex I activity and triggered 37

mitochondrial reactive oxygen species (ROS) production. The increased ROS level regulated shoot 38

regeneration by repressing expression of the genes involved in multiple pathways. Furthermore, 39

linkage disequilibrium analysis indicated that DCC1 was a major determinant of the natural 40

variation in shoot regeneration among Arabidopsis ecotypes. Thus, our study firstly uncovers a 41

novel regulatory mechanism that thioredoxin-dependent redox modification regulates de novo shoot 42

initiation via modulation of ROS homeostasis, and provides new insights into improving the 43

capacity of plant regeneration. 44

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Plant cells have the capacity to regenerate new shoots from highly differentiated tissues or organs 59

under suitable conditions, a process known as shoot regeneration (Birnbaum and Alvarado, 2008; 60

Duclercq et al., 2011). Shoot regeneration normally includes two steps (Ikeuchi et al., 2016). The 61

first step is callus formation, which is regulated by a number of transcription factors, such as 62

WUSCHEL RELATED HOMEOBOX5 (WOX5), WOX11 and WOX12 (Sugimoto et al., 2010; Liu 63

et al., 2014), PLETHORA (PLT) (Kareem et al., 2015), LATERAL ORGAN BOUNDARIES 64

DOMAIN (LBD) (Fan et al., 2010), and WOUND INDUCED DEDIFFERENTIATION 1 (WIND1) 65

(Iwase et al., 2011). The second step is shoot induction from the callus, which consists of several 66

critical events, such as the appropriate distribution of phytohormones, shoot meristem initiation and 67

organ formation (Cheng et al., 2013; Ikeuchi et al., 2016). One of the most important events in the 68

second step is the induction of the organizing center regulator WUSCHEL (WUS), which is 69

controlled by the interaction between auxin and cytokinin (Gordon et al., 2007; Cheng et al., 2013). 70

The correct distribution of auxin and cytokinin is essential for WUS induction during de novo shoot 71

regeneration (Cheng et al., 2013). Importantly, two recent studies have shown that cytokinin 72

directly activates WUS expression by the B-type ARABIDOPSIS RESPONSE REGULATORS 73

(ARRs) (Meng et al., 2017; Zhang et al., 2017). 74

Shoot regeneration is very valuable in genetic engineering and agricultural applications, but most 75

plant species cannot regenerate shoots from highly differentiated tissues or organs (Birnbaum and 76

Alvarado, 2008). Even in the same species, the shoot regeneration capacity varies among different 77

genotypes (Motte et al., 2014). However, the mechanisms underlying this natural variation in shoot 78

regeneration capacity remains unclear. Several studies have identified a few quantitative trait loci 79

related to natural variations in shoot regeneration (Schiantarelli et al., 2001; Lall et al., 2004; 80

Velázquez et al., 2004). A recent study has shown that RECEPTOR-LIKE PROTEIN KINASE1 81

(RPK1) gene is involved in natural variation in shoot regeneration capacity (Motte et al., 2014). 82

Further identification of the critical genes that control shoot regeneration and how they vary among 83

different genotypes are required for research in both the mechanisms and applications of shoot 84

regeneration. 85

Reactive oxygen species (ROS) are crucial signaling molecules that can alter their target proteins 86

activity by oxidative posttranslational modifications (Waszczak et al., 2015). Many proteins that act 87

in hormonal signal perception and response, MAPK signal transduction, and influx channel pathway, 88



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are redox sensitive to ROS (Waszczak et al., 2015; Kimura et al., 2017). Altered levels of ROS lead 89

to change the activity of these target proteins and affect various developmental processes (Schippers 90

et al., 2016). During root development, ROS homeostasis is critical for the transition from cell 91

proliferation to cell differentiation (Tsukagoshi et al., 2010). High levels of ROS result in reduced 92

root meristem activity (Tsukagoshi et al., 2010), and small leaf size (Lu et al., 2014). ROS is also 93

involved in regulating polar growth of pollen and root hairs (Mangano et al., 2016), and senescence 94

of leaf and flower (Rogers and Munné-Bosch, 2016). In addition, ROS is generated in various 95

subcellular compartments. Chloroplasts (Dietz et al., 2016), mitochondria (Huang et al., 2016), and 96

peroxisomes (Sandalio and Romero-Puertas, 2015), are the major producers of ROS in plant cells. 97

ROS homeostasis is governed by diverse antioxidant factors (Considine and Foyer, 2014; Lu and 98

Holmgren, 2014). Thioredoxins (Trxs) are key actors to modulate ROS scavenging, and functional 99

loss of Trx results in altered ROS levels (Dos Santos and Rey, 2006; Schippers et al., 2016). Trxs 100

are widely distributed proteins with a main function to reduce specific S-S group through a 101

conserved motif CxxC (Gelhaye et al., 2005; Meyer et al., 2005). Trxs alter the activity of 102

interacting target proteins via thiol-based redox modifications (Rouhier et al., 2015). A number of 103

potential Trx targets have been identified using proteomic approaches (Montrichard et al., 2009). 104

Trxs can affect diverse signaling pathways by modulating the activity of their target proteins, such 105

as enzymes of peroxiredoxins (Prxs) and glutathione peroxidase (Gpxs) for ROS scavenging (Dos 106

Santos and Rey, 2006), transcription factors for gene expression (Murmu et al., 2010; Viola et al., 107

2013), and hormonal receptors for signal transduction (Tada et al., 2008). Mitochondrial respiratory 108

chain NADH dehydrogenase complex (Complex I) consists of several essential subunits and is one 109

of the major sites of electron entry into the electron transport chain (ETC) in the process of ATP 110

production (Braun et al., 2014). Altered redox state of the subunits results in reduced Complex I 111

activity (Galkin et al., 2008). Proteomic analyses have revealed that many subunits of Complex I 112

are potential targets of Trxs, suggesting a crucial role for Trxs in regulating mitochondrial Complex 113

I function (Balmer et al., 2004; Yoshida et al., 2013; Braun et al., 2014; Dröse et al., 2014). 114

However, the evidence that Trxs directly regulate these subunits remains missing. Redox of Trxs 115

regulates diverse developmental processes, such as embryo formation, leaf development, and 116

maintenance of meristem activity (Benitez-Alfonso et al., 2009; Bashandy et al., 2010; Meng et al., 117

2010). Here, we showed that thioredoxin-dependent redox modification regulated de novo shoot 118



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initiation via modulation of ROS homeostasis. The study provides novel information for 119

understanding the mechanisms of natural variation in plant regeneration. 120

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RESULTS 122

Loss-of-Function of DCC1 Results in Inhibition of Shoot Regeneration 123

To determine the function of thioredoxins in shoot regeneration, seven T-DNA insertion mutants 124

of Trx (Trx O1, Trx O2, Trx H1, Trx H2, Trx H5, AT5G50100, AT1G52590) from the Arabidopsis 125

Biological Resource Center (ABRC) were screened, but only SALK_051222C (AT5G50100) mutant 126

showed severe defects in shoot regeneration (Supplemental Table S1). This mutant contained a 127

T-DNA insert in the fourth intron of AT5G50100 (Supplemental Fig. S1A). Reverse transcription 128

PCR (RT-PCR) analyses showed that the transcript level of this gene was decreased in this mutant 129

(Supplemental Fig. S1B), suggesting that the T-DNA insertion leads to reduced levels of functional 130

transcripts. AT5G50100 encodes a protein in the thiol-disulfide oxidoreductase family, whose 131

members contain a conserved DxxCxxC motif in their N-terminus (Ginalski et al., 2004). In 132

Arabidopsis, there exist three members with DxxCxxC motif, but their functions have not been 133

determined. Thus, At5g50100 was designated as DCC1. 134

Loss-of-function of DCC1 resulted in a decreased capacity for shoot regeneration, including the 135

low shoot regeneration frequency and the small number of shoots per callus (Fig. 1, A–C). 136

Wild-type callus generated shoots on shoot-induction medium (SIM) at 16 days (Fig. 1, A and B), 137

but the dcc1 mutant callus took 20 days to produce shoots (Fig. 1, A and B). The shoot regeneration 138

frequency in wild-type Columbia-0 (Col-0) was 100% at 28 days on SIM, while that of dcc1 was 139

about 30% (Fig. 1, A and B). The number of shoots per callus was significantly lower in dcc1 than 140

in wild type (Fig. 1, A and C). Furthermore, the phenotypes of the frequencies of shoot regeneration 141

and the shoot number per callus caused by mutation of DCC1 were both rescued by the 142

transformation of the complementary construct ProDCC1:DCC1 into dcc1 mutant (Fig. 1, A–C). 143

Thus, these results indicate that mutation of DCC1 leads to an inhibition of shoot regeneration. 144

Furthermore, we showed that DCC1 was mainly expressed in the inner region of the callus during 145

shoot regeneration by both in situ hybridization (Fig. 1D) and beta-Glucuronidase (GUS) analyses 146

(Fig. 1E). 147

DCC1 Encodes a Functional Thioredoxin Localized in Mitochondria 148

DCC1 contained an N-terminal DxxCxxC motif in a function-unknown DUF393 domain (in 149

Pfam database) (Fig. 2A). The DxxCxxC motif is a conserved signature sequence for DCC family 150



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proteins in various species, but not in animals (Fig. 2B). Phylogenetic analysis indicated that DCC1 151

shared high homology with several proteins in species, such as Camelina sativa, Brassica rapa and 152

Raphanus sativus (Fig. 2C). The presence of two cysteine residues in DxxCxxC motif implied a 153

function for DCC1 in regulating thiol-disulfide exchange. Thus, we performed a Trx activity 154



8

detection assay using fluorescein isothiocyanate-labeled insulin (FiTC-insulin). FiTC-insulin is a 155

highly sensitive substrate for the measurements of Trx activity and displays higher fluorescence 156

after disulfide reduction (Montano et al., 2014). The reduction assay was performed by incubation 157

with purified DCC1 protein and a high fluorescence intensity was achieved, whereas the control 158

without DCC1 protein showed a low level of insulin reduction (Fig. 2D), confirming its activity as a 159



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functional thioredoxin. 160

DCC1 contained a mitochondrial signal sequence, implying it might be localized in the 161

mitochondria (Fig. 2A). To test this hypothesis, we obtained a well-established marker line MT-GK 162

specially expressing GFP in mitochondria (Mito-GFP) (Nelson et al., 2007). Then, the construct 163

35S:DCC1-RFP was introduced into the MT-GK lines. The roots of the T1 seedlings were used for 164

imaging by a laser confocal microscopy. The DCC1-RFP signal was co-localized with the 165

Mito-GFP signal of the control mitochondrion marker (Fig. 2E), indicating that DCC1 is localized 166

in mitochondria. 167

DCC1 Directly Interacts with CA2 168

To uncover the functional pathway of DCC1 in shoot regeneration, we searched for its potential 169

target(s). We analyzed the published proteome-wide binary protein–protein interaction map 170

constructed by yeast two-hybrid assay in Arabidopsis thaliana, and found a DCC1 potential 171

interaction target CARBONIC ANHYDRASE 2 (CA2) (Arabidopsis Interactome Mapping 172

Consortium, 2011), which is a beta carbonic anhydrase (Soto et al., 2015). CA2, together with other 173

four carbonic anhydrases (CA1, CA3, CAL1 and CAL2), constitutes a functional subunit of 174

mitochondrial respiratory complex I (Soto et al., 2015). By a yeast two-hybrid assay, we found that 175

only the yeast co-transformed with DCC1-AD and CA2-BD constructs could survive on selection 176

medium (Fig. 3A). In pull-down assays using the purified proteins of DCC1 and CA2, an obvious 177

lane of DCC1-His was observed (Fig. 3B). To further confirm the interaction between DCC1 and 178

CA2 in vivo, we co-transformed the constructs DCC1-nLUC and CA2-cLUC into Nicotiana 179

benthamiana leaves, and observed high fluorescence intensity compared with that in the controls 180

(Fig. 3C). In DCC1-GFP immunoprecipitation assays of the F1 generation of 35S:DCC1-GFP line 181

crossed with 35S:CA2-MYC line, we detected an obvious lane of the CA2-MYC protein (Fig. 3D), 182

indicating an interaction between DCC1 and CA2. 183

Mutation of CA2 Causes the Decreased Shoot Regeneration Capacity 184

To determine the function of CA2 in shoot regeneration, we obtained the T-DNA insertion mutant 185

ca2 and analyzed its shoot regeneration capacity. The mutation of CA2 led to a significantly 186

decreased shoot regeneration capacity. During shoot regeneration, the shoots started to emerge at 16 187

days on SIM in wild type, whereas the mutant callus generated shoots at 20 days on SIM (Fig. 4A). 188

The shoot regeneration frequency of wild type reached 100% at 28 days after transfer of calli onto 189



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SIM, while that of ca2 was only about 40% (Fig. 4B). The number of shoots per callus showed a 190

similar inhibition (Fig. 4C). The frequencies of shoot regeneration and the shoot number per callus 191

were completely rescued by the transformation of the complementary construct ProCA2:CA2 into 192

the ca2 mutant (Fig. 4, A–C). Next, we crossed the two single mutants, and obtained the 193

homozygous double mutant dcc1ca2. The double mutant dcc1ca2 showed similar phenotypes with 194

those in dcc1 mutant in terms of inhibited shoot regeneration (Supplemental Fig. 2, A-C). 195

Furthermore, we detected the spatiotemporal expression patterns of CA2, and showed that CA2 196

expression in the callus started at 8 days on SIM, and gradually increased in the inner region of the 197

callus (Fig. 4, D and E). 198

Mutation of DCC1 or CA2 Leads to Reduced Complex I Activity and Increased ROS Level 199

DCC1 was a functional thioredoxin and directly interacted with CA2 protein, implying that CA2 200

might be reduced by DCC1. Therefore, we performed a reduction assay by using purified 201



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recombinant CA2 protein as the substrate. CA2 was incubated with or without GST cleaved 202

recombinant DCC1 protein. DTT (0.3mM) was added to recycle DCC1 activity. The reduction of 203

CA2 was monitored by the mobility shift in nonreducing SDS-PAGE. CA2 contained two cysteine 204

residues (Cys-83 and Cys-137) and formed dimmer and oligomer complexes by intermolecular 205

disulfide bonds (Fig. 5, A and B). The intensity of CA2 complex lanes showed significantly 206

decreased after incubation with DCC1 protein (Fig. 5, A and B), suggesting DCC1 promotes 207



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monomer formation by reduction of CA2 complex. 208

CA2 is a key subunit of the mitochondrial respiratory complex I, and defect in CA2 leads to 209

decreased activity of complex I (Soto et al., 2015). Thus, we detected the activity of respiratory 210

complex I in dcc1, ca2, and dcc1ca2 during shoot regeneration. Functional loss of DCC1 or CA2 211

caused a significantly decreased activity of the mitochondrial respiratory complex I (Fig. 5C). The 212

complex I activity in the double mutant dcc1ca2 was not more affected than that in the single 213

mutants, indicating that both proteins are acting in the same pathway. Furthermore, the reduced 214

activity of Complex I in the dcc1ca2 double mutant was completely rescued by both additions of 215

DCC1 and CA2 proteins, but not for only addition of DCC1 or CA2 (Fig. 5D). These results 216

suggest that DCC1 affects complex I activity via redox regulation of CA2 protein. Previous study 217

has shown that the impaired activity of respiratory complex I results in increased ROS levels (Soto 218

et al., 2015). Thus, we hypothesize that the reduced mitochondrial respiratory complex I activity 219

triggers mitochondrial ROS production. To test this hypothesis, we performed DAB staining assays 220

to detect the ROS levels in callus (Xie et al., 2014). During shoot regeneration, functional loss of 221

DCC1 or CA2 resulted in increased ROS levels in calli cultured on CIM and SIM, respectively (Fig. 222



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6, A and B). The ROS level in the double mutant dcc1ca2 was consistent to that in either single 223

mutant (Fig. 6, A and B). 224

ROS Levels Mediate Inhibition of Shoot Regeneration 225

Since the loss-of-function of DCC1 and CA2 resulted in increased ROS levels, we thought that 226

the inhibition of shoot regeneration in the dcc1 or ca2 mutant might be due to increased ROS levels. 227

To test this hypothesis, we treated explants of wild type with exogenous H2O2, a well-demonstrated 228



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regent responsible for increasing ROS levels (Yu et al., 2016), and found that shoot regeneration 229

was significantly inhibited in the treated explants (Fig. 7, A-C). Moreover, higher levels of H2O2 led 230

to lower shoot regeneration capacities (Fig. 7, A-C). The wild type without H2O2 treatment 231

generated visible shoots at 16 days on SIM, whereas wild type treated with 0.005‰ H2O2 and 0.01‰ 232

H2O2 generated shoots at 20 days on SIM (Fig. 7A). At 28 days on SIM, the wild type without H2O2 233

treatment had a shoot regeneration frequency of 100% (Fig. 7B), whereas wild type treated with 234

0.005‰ H2O2 and 0.01‰ H2O2 had shoot regeneration frequencies of 70% and 30%, respectively 235

(Fig. 7B). The number of shoots regenerated from wild-type calli was also decreased when treated 236

with exogenous H2O2 (Fig. 7C), indicating that ROS inhibits shoot regeneration. 237

Next, we determined whether glutathione (GSH), the main endogenous antioxidant responsible 238

for ROS removal (Lu and Holmgren, 2014), could rescue the phenotypes of dcc1 and ca2 by 239

decreased the ROS levels. The frequencies of shoot regeneration in the dcc1, ca2, and dcc1ca2 240

mutants were increased with gradually increasing concentrations of GSH (Supplemental Fig. S3A). 241

The number of shoots per callus showed similar increases under GSH treatment (Supplemental Fig. 242

S3B). The dcc1, ca2, and dcc1ca2 mutants were completely rescued by GSH at 600 µM (Fig. 8, A–243

C). Although the shoot regeneration promoted in the wild type by GSH, the shoot regeneration in 244



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the mutants of dcc1, ca2 and dcc1ca2 by GSH was significantly increased compared with that in the 245

wild type (Fig. 8, A-C). These results indicate that the reduction of ROS levels by GSH promotes 246

shoot regeneration. To further confirm the function of ROS in shoot regeneration, we transformed 247

the construct pER8-CAT3, which overexpressed CATALASE 3 (CAT3) when induced with estradiol, 248

into the Col-0, dcc1, ca2, and dcc1ca2 mutants. CAT3 encodes a catalase, which catalyzes the 249

breakdown of H2O2 into water and oxygen, thereby reduces the H2O2 level (Zou et al., 2015). The 250

CAT3 overexpression transgenic lines were obtained in the backgrounds of Col-0, dcc1, ca2, and 251

dcc1ca2, respectively (Supplemental Fig. S4). The shoot regeneration frequencies and number of 252

shoots per callus were increased in the CAT3-overexpressing transgenic lines (Fig. 8, A-C), 253

indicating that the reduction in ROS levels by overexpression of CAT3 rescued the phenotypes of 254

the mutants. CAT3 overexpression in Col-0 led to about two more shoots per callus than Col-0, 255

whereas CAT3 overexpression in dcc1, ca2 and dcc1ca2 mutants showed about five more shoots 256

compared with their mutants, respectively. Thus, the results confirm that the ROS level is critical 257



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for regulating the shoot regeneration capacity. 258

ROS Regulates Shoot Regeneration by Modulating Multiple Pathways 259

Shoot regeneration includes callus formation and shoot meristem induction. To determine 260

whether ROS was involved in regulation of callus formation by master regulators, we analyzed 261

WOXs, PLTs, LBDs and WIND1 expression during this process. Only WOX5 and WOX11 showed 262

the reduced levels in dcc1 mutant (Fig. 9A), suggesting ROS affects callus formation by modulation 263

of WOX5 and WOX11 expression. Next, we detected the WUSCHEL (WUS), SHOOT 264

MERISTEMLESS (STM) and CLAVATA3 (CLV3) which are involved in shoot meristem induction 265

(Ikeuchi et al., 2016). The transcript levels of all the three genes were decreased in dcc1 mutant 266

cultured on SIM at 12 days and 16 days (Fig. 9B), suggesting that ROS regulates shoot induction by 267

modulating expression of WOXs, WUS, CLV3 and STM. 268

To uncover the functional pathways of ROS in detail, we performed a RNA-seq analysis using 269

the calli of wild type (Col-0) and dcc1 cultured on SIM at 16 days. Three high-quality biological 270

repeats of wild type (Col-0-A, Col-0-B, Col-0-C) and dcc1 (dcc1-A, dcc1-B, dcc1-C) were used for 271

RNA-seq analyses (Supplemental Fig. S5). Using a two-fold change in the gene transcript levels 272

between the wild-type Col-0 and the mutant dcc1 with an adjusted P value (FDR) cut-off of 0.05 as 273

the criterion for differential expression, we identified many differentially expressed genes (Fig. 274

10A). Among them, 689 genes were up-regulated and 2332 genes were down-regulated in dcc1 (Fig. 275

10A; Supplemental Tables S2 and S3). Gene Ontology (GO) analyses showed that DCC1 regulated 276

multiple processes such as auxin biosynthetic process (P = 1.38 × 10-3), shoot system development 277

(P = 6.33 × 10-15), oxidation–reduction process (P = 1.83 × 10-13), cell differentiation (P = 1.98 × 278

10-11), response to hormones (P = 2.88 × 10-9), cell wall organization (P = 2.24 × 10-8), organ 279

morphogenesis (P = 1.94 × 10-7), and hydrogen peroxide catabolic process (P = 4.35 × 10-5) (Fig. 280

10B). In addition to WUS and STM, the meristem master genes KNOTTED-LIKE FROM 281

ARABIDOPSIS THALIANA1 (KNAT1), KNAT2, KNAT4 (Scofield et al., 2007), WUSCHEL 282

RELATED HOMEOBOX (WOXs) (van der Graaff et al., 2009), and CUP-SHAPED COTYLEDON 283

(CUCs) (Ikeuchi et al., 2016), were down-regulated in dcc1 (Fig. 10, B and C). Next, we performed 284

quantitative reverse transcription PCR (qRT-PCR) to confirm the transcript levels of genes 285

identified in the RNA-seq analyses. As expected, the transcript levels of these genes were low in 286

dcc1 mutant, and in the presence of exogenous H2O2 (Fig. 10D; Supplemental Fig. S6). These 287



17

results suggest that DCC1-mediated ROS level regulates shoot regeneration by the genes involved 288

in shoot meristem initiation. 289

Interestingly, several auxin biosynthetic genes, including TRYPTOPHAN AMINOTRANSFERASE 290

OF ARABIDOPSIS 1 (TAA1), YUCCA2 (YUC2), YUC4, YUC5, and YUC9 (Zhao, 2010) were 291



18

significantly down-regulated in dcc1 (Fig. 10, C and D; Supplemental Fig. S6). The transcript levels 292

of auxin response genes, such as GRETCHEN HAGEN 3.6 (GH3.6) and SMALL AUXIN 293

UPREGULATED 51 (SAUR51) (Hagen and Guilfoyle, 2002; Staswick et al., 2005), were also 294



19

decreased in dcc1 (Fig. 10, C and D; Supplemental Fig. S6). Further, we used the 295

well-demonstrated auxin marker DR5rev:GFP to detect the auxin response signal distribution in 296

regenerating shoots (Cheng et al., 2013). The GFP signal was weakened by H2O2 treatment during 297

shoot regeneration (Fig. 10E). Auxin is a critical determinant in shoot regeneration, and the 298

impaired auxin biosynthesis and signaling repress shoot regeneration (Gordon et al., 2007; Cheng et 299

al., 2013). Moreover, the functional loss of DCC1 led to increased ROS levels (Fig. 6, A and B), and 300

ROS repressed auxin signaling (Fig. 10E). Thus, we propose that DCC1-mediated ROS level 301

regulates shoot regeneration, at least in part, through a modulation of the auxin biosynthesis and 302

signaling pathway. 303

DCC1 Is a Major Determinant of Natural Variation in Shoot Regeneration 304

To determine whether DCC1 was a factor in the natural variation in shoot regeneration, 305

forty-eight ecotypes of Arabidopsis were used in shoot regeneration analyses using the roots as 306

explants. The shoot regeneration capacity varied widely among the different ecotypes of 307

Arabidopsis. The shoot regeneration frequencies ranged from 5% to 100% (Supplemental Fig. S7A). 308

The ecotypes Gu-0, Nc-1, Wa-1, and Kelsterbach-4 showed very low shoot regeneration frequencies 309

on SIM at 28 days, while the ecotypes Col-0, Ws-0, Pu2-7, Lan-0, and Bu-0 showed high shoot 310

regeneration frequencies (Supplemental Fig. S7A). These diverse frequencies indicated the wide 311

natural variation in regeneration capacity among Arabidopsis genotypes. There was also a wide 312

range among genotypes in the number of shoots per callus (Supplemental Fig. S7B). Each callus of 313

Col-0, Ws-0, Pu2-7, Bu-0, Tsu-1 and Ct-1 generated more than five shoots, while calli of other 314

ecotypes generated four or fewer. The results confirm that there are diverse shoot regeneration 315

capacities among different ecotypes of Arabidopsis. 316

We further performed linkage disequilibrium analyses using the nucleotide sequences of DCC1 in 317

48 different ecotypes, and found that six SNPs (SNP 108, 147, 174, 175, 378, and 481) were highly 318

associated with the shoot regeneration frequency (Fig. 11A). Two haplotypes (Hap1 and Hap2) of 319

DCC1 were identified among 48 natural variants of Arabidopsis. Hap1 included 30 ecotypes such 320

as Col-0, Ws-0, Pu2-7, Lan-0, and Bu-0, and Hap2 included 18 ecotypes such as Gu-0, Nc-1, 321

Keleterbach-4, Hn-0, Su-0 (Fig. 11, A-C). The shoot regeneration frequencies and the number of 322

shoots per callus were much higher in the Hap1 than in the Hap2 ecotypes (Fig. 11, D and E), 323

suggesting that this natural variation in DCC1 is related to the regulation of shoot regeneration. 324



20

Among the six SNPs, only two (SNP 175 and 481) resulted in the sense mutation (I59V and I161V) 325

for the corresponding amino acids (Fig. 11, B and C). To identify the critical SNPs in DCC1 among 326

the natural variants, we detected the Trx activity by reduction of FiTC-insulin. Mutations at both 327

175 and 481 sites did not affect Trx activity of DCC1 (Fig. 11, F and G). Next, we performed yeast 328



21

two-hybrid assays using the DCC1 with mutations at 175 and 481 sites. We found that DCC1 did 329

not interact with CA2 when there were mutations at both sites 175 and 481 (Fig. 11H). We also 330

transformed a pDCC1:DCC1-m175-m481 construct with DCC1 mutated at 175 and 481 sites to 331

rescue dcc1 mutant. The shoot regeneration frequencies in the pDCC1:DCC1-m175-m481-dcc1 332

transgenic lines were not significantly different from those in dcc1 (Fig. 11I), implying that SNP 333

175 and SNP 481 of DCC1 are critical for shoot regeneration. 334

Because DCC1 regulated shoot regeneration through ROS level, we assumed that 335

DCC1-mediated ROS homeostasis might be involved in the natural variation in shoot regeneration 336

among Arabidopsis ecotypes. To test this hypothesis, we detected the ROS levels in the Hap1 and 337

Hap2 ecotypes by DAB staining (Fig. 12, A and B). The shoot regeneration frequencies and the 338

number of shoots per callus were higher in the Hap1 ecotypes (Col-0, Kro-0, En-1, Ct-1, and Lp2-6) 339

than in the Hap2 ecotypes (Bsch-0, Aa-0, Hn-0, Kelsterbach-4, and Gu-0) (Fig. 12, C and D). 340

Interestingly, the ROS levels were significantly lower in the Hap1 ecotypes than in the Hap2 341

ecotypes (Fig. 12E). These results suggest that DCC1-mediated ROS homeostasis is critical to the 342

natural variation in shoot regeneration among Arabidopsis ecotypes. 343

344



22

DISCUSSION 345

Trxs belong to small proteins with a conserved CxxC motif throughout all organisms (Gelhaye 346

et al., 2005; Meyer et al., 2005). Classic Trxs, such as Trx m, Trx o, Trx h and Trx f, contain a motif 347

of WCGPC or WCPPC, and atypical Trxs, such as APS REDUCTASE 1 (APR1), and HIGH 348

CHLOROPHYLL FLUORESCENCE 164 (HCF164), have a motif of WCPFC, HCGPC or 349

WCEVC (Gelhaye et al., 2005; Meyer et al., 2005). Trxs catalyze the reduction of disulfide bond 350

through these motifs and are critical to change redox state of their target proteins (Rouhier et al., 351

2015). Redox state of ND3 (an important subunit of Complex I) determines activity of Complex I 352

(Galkin et al., 2008). Many subunits of mitochondrial respiratory Complex I (such as NAD7, NAD9, 353

NDS8A, and NDUV2) are identified as potential targets of Trxs, but the direct evidence of redox 354

regulation of these subunits by Trxs is missing (Balmer et al., 2004; Yoshida et al., 2013). In this 355

study, we characterized a novel atypical Trx DCC1, which belongs to DCC family proteins. These 356

proteins contain a conserved DxxCxxC motif (such as DGDCPLC, DGECPLC and DGVCHLC) 357

that differs from motifs of classic and atypical Trxs (Fig. 2B). DCC1 had the Trx activity 358

determined by reduction of insulin (Fig. 2D). CA2 is an essential subunit of Complex I (Soto et al., 359

2015), and was identified as a direct target of DCC1 (Fig. 5, A and B). DCC1 regulated Complex I 360

activity by reduction of CA2 complex (Fig. 5, A-D). Inhibition of Complex I activity caused by 361

mutation of DCC1 or CA2 triggered the increased ROS production (Fig. 6, A and B), suggesting 362



23

that DCC1 regulates Complex I activity and ROS homeostasis by redox regulation of CA2. 363

Many studies show that ROS can act as signaling factors regulating diverse processes (Rouhier et 364

al., 2015; Schmidt and Schippers, 2015; Schippers et al., 2016). NADPH-DEPENDENT 365

THIOREDOXIN REDUCTASE A (NTRA), NADPH-DEPENDENT THIOREDOXIN REDUCTASE B 366

(NTRB), and glutathione biosynthesis gene CADMIUM SENSITIVE 2 (CAD2) function to maintain 367

ROS homeostasis, and the triple mutant ntra ntrb cad2 generated an abnormal shoot meristem 368

(Bashandy et al., 2010). Higher levels of ROS caused by overexpression of UP BEAT1 (UPB1) led 369

to a short root meristem (Tsukagoshi et al., 2010). Elevated levels of ROS by the mutation of 370

KUODA1 (KUA1) led to the decreased leaf cell size (Lu et al., 2014). Here, we showed that 371

increasing level of ROS resulted in the inhibition of shoot regeneration (Fig. 6, A and B; Fig. 7, A–372

C), whereas decreasing level of ROS level increased the capacity of shoot regeneration in the 373

mutants of dcc1, ca2, and dcc1ca2 (Fig. 8, A–C). Thus, ROS homeostasis is critical for regulation 374

of shoot regeneration. 375

Different mechanisms have been proposed to mediate perception of ROS (Wrzaczek et al., 2013). 376

An important mechanism is the one-component redox signaling system, which is based on 377

redox-sensitive transcription factors (Schmidt and Schippers, 2015). Recent studies have identified 378

a number of crucial redox-sensitive transcription factors, such as (PHAVOLUTA) PHV for 379

meristem development and organ polarity, BASIC REGION/LEUCINE ZIPPER 380

TRANSCRIPTION FACTOR 16 (bZIP16) for light signaling, and TEOSINTE 381

BRANCHED1-CYCLOIDEAPCF 15 (TCP15) for auxin signaling (Schmidt and Schippers, 2015). 382

Our results indicated that the increased ROS levels resulted in repressed expression of master genes 383

for callus formation (WOX5, WOX11), and shoot meristem initiation (WUS, CLV3 and STM) (Fig. 9, 384

A and B). Moreover, auxin biosynthesis genes (YUC4, TAA1) were repressed by ROS (Fig. 10, C 385

and D). Previously, it was shown that auxin was critical for shoot induction, and mutation of auxin 386

biosynthetic genes YUCs repressed shoot regeneration (Gordon et al., 2007; Cheng et al., 2013). 387

The redox-sensitive transcription factors TCPs regulate YUCs expression and auxin biosynthesis 388

(Viola et al., 2013; Lucero et al., 2015; Challa et al., 2016). Thus, it is likely that ROS regulates 389

shoot regeneration by redox modification of transcription factors involved in auxin biosynthesis and 390

signaling. 391

The evolutionary adaptation of plants to environmental changes leads to diverse natural variation, 392



24

which is critical for plant diversity (Mitchell-Olds and Schmitt, 2006). Natural variation causes a 393

wide range of biological phenotypes and provides rich resources to analyze many important 394

complex traits (Mitchell-Olds and Schmitt, 2006). A number of factors involved in natural 395

variations have been identified in diverse biological processes including regulation of flowering, 396

seed development, and drought resistance (Johanson et al., 2000; Li et al., 2011b; Wang et al., 2016). 397

FRIGIDA (FRI) is a major determinant of the natural variation in Arabidopsis flowering time 398

(Johanson et al., 2000). Natural variations in GS5 can explain variations in rice grain size and yield 399

(Li et al., 2011b), and those in ZmVPP1 contribute to the drought tolerance trait in Zea mays (Wang 400

et al., 2016). Here, we identified a major regulator DCC1 that explains the variation in shoot 401

regeneration capacity among natural variants of Arabidopsis (Fig. 11, A–E). The polymorphisms of 402

DCC1 were used to classify the different ecotypes of Arabidopsis into two groups: Hap1 and Hap2 403

(Fig. 11B). Interestingly, mutations at both two critical SNPs (SNP 175, SNP 481) did not affect the 404

Trx activity of DCC1 (Fig. 11G), but blocked the interaction between DCC1 and CA2 (Fig. 11H), 405

indicating that the two SNPs are critical for the function of DCC1, which is a major player in 406

determining shoot regeneration capacity among natural variations. 407

MATERIALS AND METHODS 408

Plant Materials 409

The mutants dcc1 (SALK_051222C), ca2 (SALK_010194C), MT-GK line (CS16263), and 410

different ecotypes of Arabidopsis were obtained from the Arabidopsis Biological Resource Center 411

(ABRC). DR5rev:GFP lines were generously provided by Dr. Jian Xu (Department of Biological 412

Science, National University of Singapore) (Xu et al., 2006). 413

Shoot Regeneration 414

Shoot regeneration experiment was performed as described previously (Li et al., 2011a). Seeds 415

were placed on germination medium after sterilization in 70% v/v ethanol for 5 min and 2.6% v/v 416

sodium hypochlorite for 10 min. All the seeds were stratified at 4°C for 3 days, and then grown for 417

12 days in a growth chamber at 22°C under a 16-h light/8-h dark photoperiod. Root segments (5–10 418

mm) were cut and placed on callus induction medium CIM (Gamborg’s B5 medium supplemented 419

with 0.5 g/L MES, 2% w/v glucose, 0.2 µM kinetin, 2.2 µM 2,4-dichlorophenoxyacetic acid, and 420

0.8% w/v agar). After the explants were incubated in continuous light for 6 days, the calli were 421

transferred onto SIM (Gamborg’s B5 medium supplemented with 0.5 g/L MES, 2% w/v glucose, 422



25

0.9 µM 3-indoleacetic acid, and 0.5 µM 2-isopentenyladenine, 0.8% w/v agar), and incubated in 423

continuous light. The calli were transferred onto fresh medium every 6 days. Images of calli were 424

acquired using an Olympus DP72 microscope. The shoots on each callus were defined as being at 425

least 2 mm long. Shoot regeneration frequency (%) was calculated as follows: number of calli with 426

at least one shoot / total number of calli cultured on SIM × 100. Three sets of biological replicates 427

were used in the calculations and more than 100 calli were examined in each replicate. 428

Plasmid Construction 429

The oligonucleotide primers for all constructs are given in Supplemental Table S4. For 430

phenotypic complementation and GUS signal analyses, DCC1 or CA2 genomic fragments including 431

the promoter and gene were introduced into pMDC99 to construct the ProDCC1:DCC1 and 432

ProCA2:CA2, respectively, and into the pMDC163 to obtain ProDCC1:DCC1-GUS and 433

ProCA2:CA2-GUS, respectively. For subcellular localization, DCC1 cDNA was cloned into 434

pH7RWG2 to generate 35S:DCC1-RFP by Gateway Technology (Karimi et al., 2002). For the yeast 435

two-hybrid constructs, cDNAs of DCC1 and CA2 without the signal peptide sequence were cloned 436

into the pGADT7 and pGBKT7 to generate DCC1-AD and CA2-BD, respectively. For the pull-down 437

assay, cDNAs of DCC1 and CA2 without the signal peptide sequence were cloned into pET28a and 438

pGEX-4T-1 to generate DCC1-His and CA2-GST, respectively. For the firefly luciferase 439

complementation assay, gene sequences of DCC1 and CA2 were cloned into p1300-nLUC and 440

p1300-cLUC to generate 35S:DCC1-nLUC and 35S:CA2-cLUC, respectively. For the 441

co-immunoprecipitation, gene sequences of DCC1 and CA2 were introduced into pEarlyGate103 442

and pEarlyGate203 to generate 35S:DCC1-GFP and 35S:CA2-MYC, respectively. For the reduction 443

of CA2, cDNA of DCC1 without the signal peptide sequence was cloned into pGEX-4T-1 to 444

generate DCC1-GST. For CAT3-overexpression, CAT3 cDNA was amplified and cloned into the 445

pER8 to construct pER8-CAT3. 446

For the construct pDCC1:DCC1-m175-m481, DCC1 promoter sequence was amplified using 447

the primer DCC1-F7/R7 and cloned into pBI121. DCC1-m175-m481 (m175 indicates mutation at 448

175 site of DCC1 gene) fragments were amplified using primers (DCC1-F8/R8, DCC1-F9/R9, 449

DCC1-F10/R10) by over-lap-extension two-step PCR mutagenesis method, and introduced into the 450

pBI121 containing DCC1 promoter. For DCC1 Trx activity determination, DCC1-m175-His (with 451

primer DCC1-F11/R11), DCC1-m481-His (with primers DCC1-F12/R12, DCC1-F13/R13), and 452



26

DCC1-m175-m481-His (with primers DCC1-F11/R12, DCC1-F13/R13) were generated by 453

over-lap-extension two-step PCR mutagenesis and inserted into pET28a for protein purification. For 454

yeast hybrid interaction, DCC1-m175-AD (with primer DCC1-F14/R14), DCC1-m481-AD (with 455

primers DCC1-F15/R15, DCC1-F16/R16), and DCC1-m175-m481-AD (with primers 456

DCC1-F14/R15, DCC1-F16/R16) were amplified by over-lap-extension two-step PCR mutagenesis 457

and inserted to pGADT7 for yeast hybrid interaction. 458

GUS Staining Assay 459

We conducted GUS staining assays as described elsewhere (Sieburth and Meyerowitz, 1997; Su 460

et al., 2009). Briefly, calli were incubated in GUS assay buffer at 37°C for 10 h, and fixed in 70% 461

v/v ethanol at room temperature. The calli were embedded in paraffin and cut into 10-μm sections. 462

Ruthenium red (0.2 g/L) was used to stain cell walls. 463

Confocal Microscopy 464

MT-GK is a reported marker line specially expressing GFP in mitochondria (Mito-GFP) (Nelson 465

et al., 2007). To determine the subcellular localization of DCC1, the construct 35S:DCC1-RFP was 466

introduced into MT-GK lines. The roots of the T1 transgenetic lines were excised for imaging by a 467

Leica TCS SP5 confocal microscope. The DCC1-RFP signal was observed at 505–550 nm emission 468

after 561 nm excitation, whereas, the Mito-GFP signal was observed at 570–620 nm emission after 469

488 nm excitation. The merged signals of GFP and RFP showed yellow color. To detect the auxin 470

response pattern, approximately 60 calli cultured on SIM at different times were sampled to observe 471

the expression of DR5rev:GFP. The calli were cut into 1–2 mm sections along the longitudinal axis, 472

and the sections were viewed under a Leica TCS SP5 confocal microscope (Leica, Germany). The 473

GFP signal was observed at emission 505–550 nm after 488 nm excitation. 474

Phylogenetic Analysis 475

Phylogenetic analysis was used DCC1 (NP_568719.1) with its homologs in Camelina sativa 476

(XP_010441588.1), Brassica rapa (XP_010441588.1), Raphanus sativus (XP_018455194.1), 477

Gossypium hirsutum (XP_016755751.1), Ziziphus jujuba (XP_015882648.1), Malus domestica 478

(XP_008393058.1), Prunus persica (XP_007209569.1), Oryza officinalis (XP_015633461.1), Zea 479

mays (XP_008663715.1), Physcomitrella patens (XP_001777984.1), Populus trichocarpa 480

(XP_002322151.2), Vitis vinifera (XP_002283569.1), Triticum urartu (EMS60538.1), Microcystis 481

aeruginosa (WP_002792509.1), Arabidopsis thaliana (AT1G52590, NP_564611.1), Arabidopsis 482



27

thaliana (AT1G24095, NP_001185076.1), Caulobacter crescentus (NP_422377.1), Bacillus 483

halodurans (WP_010897025.1), and Pseudomonas aeruginosa (NP_249825.1). The analysis was 484

performed by MEGA 5.1 software. The protein sequences were downloaded from database of 485

National Center for Biotechnology Information (NCBI). 486

Thioredoxin Activity Assay 487

The construct pET28a-DCC1 was transferred into Rosetta competent cells. DCC1-His proteins 488

were induced by incubation in 1 mM IPTG at 22°C with shaking at 120 rpm for 16 h. The cell pellet 489

was resuspended in buffer (25 mM Tris, pH 7.5, 0.5 mM dithiothreitol [DTT]) (Motohashi et al., 490

2003). Protein purification was performed using Ni Sepharose 6 Fast Flow (GE Healthcare, 491

Piscataway, NJ, USA, catalog number 28-9355-97). Then, the proteins were dialyzed against buffer 492

(25 mM Tris, pH 7.5) to remove imidazole using Slide-A-Lyzer Dialysis Cassettes (ThermoFisher 493

Scientific, Rockford, IL, USA, catalog number 66810) for 24 h. Trx activity was measured using 494

the Thioredoxin Activity Fluorescent Assay Kit (Cayman Chemicals, Ann Arbor, MI, USA, catalog 495

number 11527). The fluorescein isothiocyanate-labeled insulin (FiTC-insulin) in the kit was used as 496

the substrate of DCC1. FiTC displays higher fluorescence after disulfide reduction (Montano et al., 497

2014). The reduction assay was performed by incubation with purified DCC1 protein (10 μg). 498

NADPH and TrxR were used to recycle the DCC1 Trx activity. The reaction mixture without DCC1 499

proteins was used as the control. The fluorescence intensity of each sample was recorded at 515–500

525 nm emission after excitation at 480–495 nm for 60 minutes using a BioTek Synergy™ 2 501

Multi-Mode Reader (BioTek, Winooski, VT, USA) at ambient room temperature. Three sets of 502

biological replicates were performed for each reaction. 503

Yeast Two-Hybrid Assay 504

The yeast two-hybrid assay was performed using the Matchmaker Gold Yeast Two-Hybrid 505

System (Clontech, Palo Alto, CA, USA, catalog number 630489) according to the manufacturer’s 506

instructions. The constructs DCC1-AD and CA2-BD were co-transferred into Y2H Gold competent 507

cells. Activation was observed at 3 days on selection plates (SD/ - Leu - Trp - His - Ade) with 508

X-α-gal. 509

Firefly Luciferase Complementation Assay 510

Firefly luciferase complementation assays were conducted as described previously (Li et al., 511

2014). The constructs DCC1-nLUC and CA2-cLUC were transformed into the leaf of N. 512



28

benthamiana for transient expression. Transfected leaves were sprayed with buffer (1 mM 513

D-luciferin sodium salt, 0.1% Triton X-100) 5 min before being imaged using the IVIS Lumina II 514

system (Caliper Life Sciences, Hopkinton, MA, USA). 515

Pull-Down Assay 516

For the pull-down assay, 10 μg CA2-GST protein was incubated with 10 μL 517

glutathione-Sepharose-4B beads (GE Healthcare; catalog number 17-0756-01) in blocking buffer 518

(140 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1% w/v NP-40, 1 g BSA) 519

under agitation at 4°C for 2 h. 1 μg DCC1-His protein was added, and the mixture was incubated 520

for 2 h in binding buffer (140 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1% 521

w/v NP-40). The beads were washed 10 times with washing buffer (400 mM NaCl, 2.7 mM KCl, 10 522

mM Na2HPO4, 1.8 mM KH2PO4, 0.1% w/v NP-40). Finally, 10% input and pull-down proteins 523

were separated by 12% SDS-PAGE and detected by immunoblotting using the antibodies anti-His, 524

diluted 1:3000 (Sigma, St Louis, MO, USA; catalog number H1029) or anti-GST, diluted 1:3000 525

(Sigma; catalog number G1160). 526

Co-Immunoprecipitation Assay 527

We used transgenic seedlings of 35S:DCC1-GFP and the F1 generation of 35S:DCC1-GFP × 528

35S:CA2-MYC for immunoprecipitation analyses. Proteins were extracted from 2 g seedlings with 529

extraction buffer (140 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1 mM EDTA, 530

0.1% w/v NP-40, 5 mM DTT, 0.5 mM PMSF). Then, 60 μL beads were incubated with 10 μL 531

anti-GFP antibody with agitation for 2 h at 4°C. Then, supernatants were added and incubated with 532

agitation for 8 h at 4°C. After incubation, beads were washed 10 times with washing buffer (400 533

mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1 mM EDTA, 0.1% NP-40, 5 mM 534

DTT, 0.5 mM PMSF). Finally, 10% input and immunoprecipitation proteins were separated by 12% 535

SDS-PAGE and detected by immunoblotting using the antibodies anti-MYC, diluted 1:1000 (Sigma; 536

catalog number M4439) or anti-GFP, diluted 1:1000 (Roche, Mannheim, Germany; catalog number 537

11814460001). 538

Reduction of CA2 by DCC1 539

The reduction assay was performed as described previously with slight modifications (Yoshida et 540

al., 2015). The GST tag of the recombinant DCC1-GST proteins was cleaved by a thrombin (Sigma; 541

catalog number T9326). Purified CA2-His protein (1μM) was incubated with GST-cleaved DCC1 542



29

protein in the assay mixture containing 50 mM Tris-HCl (pH 7.5), 50 mM NaCl. DTT (0.3 mM) 543

was added to recycle DCC1 Trx activity. The mixture without DCC1 proteins was used as the 544

control. After incubation for 30 min at 25 °C, proteins were subjected to non-reducing (without 545

2-mercaptoethanol) or reducing (with 2-mercaptoethanol) SDS-PAGE followed by immunoblot 546

analysis using Anti-His antibody diluted 1:5000 (Sigma, catalog number H1029). 547

Mitochondrial Respiratory Complex I Activity Assay 548

Calli (0.1 g) of wild type (Col-0), dcc1, ca2, and dcc1ca2 cultured on SIM at 16 days were 549

collected, and then the mitochondria were isolated using a Plant Mitochondria Isolation Kit (Biohao, 550

Wuhan, China; catalog number P0045) according to the manufacturer’s instructions. Mitochondrial 551

respiratory complex Ⅰ activity was determined using 20 μg mitochondrial protein with a MitoCheck 552

Complex Ⅰ Activity Assay Kit (Cayman; catalog number 700930). The absorbance of all samples 553

was measured at 340 nm for 60 min using a plate reader. Complex Ⅰ activity was calculated from the 554

decrease in absorbance per minute. Standard errors were calculated from three sets of biological 555

replicates. 556

Chemical Treatments 557

Chemical reagents were added to the medium before transfer of calli, and calli were transferred to 558

new medium with fresh reagents every 6 days. Different concentrations of H2O2 (0.005‰, 0.01‰) 559

or GSH (100 μM, 300 μM and 600 μM) were added to the shoot regeneration system, and 10 μM 560

estradiol was added to induce the transcription of CAT3 to complement the phenotypes of dcc1, ca2, 561

and dcc1ca2. 562

DAB Staining Assay 563

Calli were incubated in DAB staining buffer (50 mM Tris, pH 7.6, 0.6 mg/mL DAB) at room 564

temperature in darkness, and then fixed in 70% v/v ethanol at room temperature. The calli were 565

observed under an Olympus DP72 microscope until the chlorophyll disappeared. The relative DAB 566

staining intensity was analyzed by Image J software. Three sets of biological replicates were 567

calculated and more than 30 calli were examined in each replicate. 568

Quantitative Real-Time PCR 569

Total RNA was isolated using TRI Reagent® (Sigma; catalog number T9424), and treated with 570

DNase Ι (Thermo Fisher Scientific, San Jose, CA, USA; catalog number EN0521). Then, cDNAs 571

were synthesized using M-MLV reverse transcriptase (Promega, Madison, WI, USA; catalog 572



30

number M1701). The qRT-PCR assays were conducted using a Bio-Rad CFX96 Real-Time PCR 573

Detection System (Bio-Rad, Hercules, CA, USA) in a 20-µL reaction volume with 45 cycles. The 574

cDNA levels were normalized against those of two housekeeping genes; TUBILIN2 (TUB2) and 575

ACTIN2 (ACT2). The relative expression level of each gene was standardized to TUB2 and 576

calculated using the comparative CT method (Schmittgen and Livak, 2008). Mean values were 577

calculated from three biological replicates. The sequences of primers used for qRT-PCR are listed in 578

Supplemental Table S4. 579

RNA Sequencing and Data Analyses 580

Three biological repeats of wild type (Col-0-A, Col-0-B and Col-0-C) and mutants dcc1 (dcc1-A, 581

dcc1-B and dcc1-C) were used for RNA sequencing. Total RNAs were isolated from the calli of 582

wild type Col-0 and dcc1 cultured on SIM at 16 days with TRI reagent (Sigma; catalog number 583

T9424). RNA was sequenced using the Illumina 2500 instrument in Gene Denovo Biotechnology 584

Co. (Guangzhou, China). The raw reads were aligned to the genome sequences of TAIR10 585

(www.arabidopsis.org) using Tophat2 software (version 2.0.3.12) (Kim et al., 2013). The gene 586

expression levels were measured in FPKM using Cufflinks software (Trapnell et al., 2014). 587

Statistical analyses were performed using the edgeR package (http://www.rproject.org/). 588

Differentially expressed genes were those with a fold change ≥ 2 and a false discovery rate (FDR) 589

<0.05 between the wild-type Col-0 and the mutant dcc1. A GO enrichment analysis was performed 590

in the Gene Ontology database (http://www.geneontology.org/) (Botstein et al., 2000). The RNA 591

sequencing data are available in the ArrayExpress database (www.ebi.ac.uk/arrayexpress) under the 592

accession number E-MTAB-5236. 593

Linkage Disequilibrium Analyses 594

Linkage disequilibrium analyses were performed using Genome Variation Server (GVS) (Carlson 595

et al., 2004) with DCC1 nucleotide sequences from 48 ecotypes of Arabidopsis. 596

Accession Numbers 597

Sequence data from this article can be found in the GenBank/EMBL data libraries under accession 598

numbers AT5G50100 (DCC1), AT1G47260 (CA2), , AT3G11260 (WOX5), AT3G03660 (WOX11), 599

AT5G17810 (WOX12), AT5G10510 (PLT3), AT5G57390 (PLT5), AT2G42430 (LBD16), 600

At2G42440 (LBD17), At2G45420 (LBD18), At3G58190 (LBD29), AT1G78080 (WIND1), 601

AT2G17950 (WUS), AT2G27250 (CLV3), AT1G62360 (STM). 602



31

Supplemental Data 603

Supplemental Figure S1. Identification of dcc1 mutant. 604

Supplemental Figure S2. Phenotypes of double mutant dcc1ca2 during shoot regeneration. 605

Supplemental Figure S3. Exogenous GSH promotes shoot regeneration. 606

Supplemental Figure S4. Transcript level of CAT3 in CAT3-overexpressing transgenic lines. 607

Supplemental Figure S5. Correlations among three biological repeats of RNA-seq analyses. 608

Supplemental Figure S6. Analyses of differentially expressed genes identified by RNA-seq were 609

confirmed by qRT-PCR. 610

Supplemental Figure S7. Shoot regeneration capacity of different Arabidopsis ecotypes. 611

Supplemental Table S1. Frequencies of shoot regeneration in the Trx mutants. 612

Supplemental Table S2. Up-regulated genes in dcc1 mutant as determined by RNA-seq analyses. 613

Supplemental Table S3. Down-regulated genes in dcc1 mutant as determined by RNA-seq 614

analyses. 615

Supplemental Table S4. Sequences of primers used in this study. 616

ACKNOWLEDGEMENTS 617

We thank all who generously provided plant materials in this research. We thank Dr. Min Ni 618

(Department of Plant Biology, University of Minnesota) for his critical reading of this manuscript. 619

620

Figure 1. Shoot regeneration is inhibited in dcc1 mutant. A to C, Callus morphology (A), 621

frequencies of shoot regeneration from calli (B), and number of shoots per callus (C) in wild type 622

(Col-0), dcc1, and dcc1 ProDCC1:DCC1 cultured on SIM at indicated times. D, Expression pattern 623

of DCC1 detected by in situ hybridization in calli of Col-0 at indicated times on SIM. E, Expression 624

pattern of DCC1 detected by GUS staining in calli of ProDCC1:DCC1-GUS transgenetic lines at 625

indicated times on SIM. S0 represents calli cultured on callus-induction medium (CIM) at 6 days 626

using roots as explants before transfer to SIM. S8, S12, S16, S20, S24 and S28 indicate calli 627

cultured on SIM at 8, 12, 16, 20, 24 and 28 days, respectively. Standard errors were calculated from 628

three sets of biological replicates and more than 100 calli were examined in each replicate. Scale 629

bars = 500 µm. Significant difference, **p < 0.01 (Student’s one-tailed t test). 630

Figure 2. DCC1 is a functional Trx localized in mitochondria. A, Models of DCC1 protein with a 631

mitochondria signal sequence predicted in UniProt database and a conserved DxxCxxC motif in a 632



32

function-unknown DUF393 domain analyzed in Pfam database. B, Alignment of the amino acid 633

sequences of different DCC family proteins. The DxxCxxC motif is a conserved signature sequence 634

for DCC family proteins in various species. The NCBI accession numbers of proteins in different 635

species are presented in Materials and Methods in detail. C, Phylogenetic analyses of DCC1 with its 636

homologs in various species. DCC1 shares high homology with several proteins in species, such as 637

Camelina sativa, Brassica rapa and Raphanus sativus. D, Insulin reduction by recombinant DCC1 638

proteins. Purified DCC1 proteins were subjected to a reduction assay by using fluorescein 639

isothiocyanate-labeled insulin (FiTC-insulin) as the substrate, which displayed higher fluorescence 640

after disulfide reduction. The assay mixture lacking recombinant DCC1 proteins served as the 641

control. Fluorescence intensity was recorded at 515-525 nm emission after 480-495 nm excitation 642

for 120 minutes in a fluorescent plate reader at room temperature. E, Subcellular localization of 643

DCC1. MT-GK is a well-established marker lines specially expressing GFP in mitochondria 644

(Mito-GFP). The construct 35S:DCC1-RFP was transformed into MT-GK lines. The T1 645

transgenetic lines roots were excised for imaging by a confocal microscope. The DCC1-RFP signal 646

(E1) was observed at 505–550 nm emission after 561 nm excitation, whereas, the Mito-GFP signal 647

(E2) was observed at 570–620 nm emission after 488 nm excitation. The merged signals of GFP 648

and RFP showed yellow color (E3), indicating DCC1 is localized in mitochondria. Scale bars = 20 649

µm. 650

Figure 3. DCC1 interacts with CA2. A, Interaction between DCC1 and CA2 in yeast two-hybrid 651

assay. Activation was observed at 3 days on selection plates (SD/ - Leu - Trp - His - Ade) with 652

X-α-gal. B, Interaction between DCC1 and CA2 in pull-down assay. 10% Input and GST-pull-down 653

proteins were detected by immunoblotting using anti-His antibody, respectively (upper gels). 654

CA2-GST and GST proteins were detected by immunoblotting using anti-GST antibody (lower gel). 655

C, Interaction between DCC1 and CA2 in firefly luciferase complementation assays in transiently 656

transfected leaf of N. benthamiana. D, Interaction between DCC1 and CA2 in 657

co-immunoprecipitation assays. 10% Input and immunoprecipitated proteins with anti-GFP were 658

detected by immunoblotting using an anti-MYC antibody, respectively (upper gels). 10% Input and 659

DCC1-GFP proteins were detected by immunoblotting using an anti-GFP antibody, respectively 660

(lower gels). 661

Figure 4. Loss-of-function of CA2 caused the decreased capacity of shoot regeneration. A to C, 662



33

Callus morphology (A), frequencies of shoot regeneration from calli (B) and number of shoots per 663

callus (C) in wild type (Col-0), ca2, and ca2 ProCA2:CA2 cultured on SIM at indicated times. D, 664

Expression pattern of CA2 detected by in situ hybridization in calli of Col-0 at indicated times on 665

SIM. E, Expression pattern of CA2 detected by GUS staining in calli of ProCA2:CA2-GUS 666

transgenetic lines at indicated times on SIM. S0 represents calli cultured on CIM at 6 days using 667

roots as explants before transfer to SIM. S8, S12, S16, S20, S24 and S28 indicate calli cultured on 668

SIM at 8, 12, 16, 20, 24 and 28 days, respectively. Standard errors were calculated from three sets 669

of biological replicates and more than 100 calli were examined in each replicate. Scale bars = 500 670

µm. Significant difference, **p < 0.01 (Student’s one-tailed t test). 671

Figure 5. DCC1 regulates complex I activity via CA2 protein. A and B, CA2 dimmer and oligomer 672

were reduced by DCC1. Purified CA2-His protein was incubated in the assay mixture with or 673

without DCC1 GST-cleaved protein (5 μM) for 30 min at room temperature and then subjected to 674

nonreducing (A) or reducing (B) SDS-PAGE followed by immunoblot analysis. DTT (0.3 mM) was 675

added to recycle DCC1 Trx activity. The position of the monomer, dimmer and oligomer of CA2 are 676

indicated. CA2 dimmer and oligomer showed significantly reduced levels when incubated with 677

DCC1 proteins (right lane). The reaction mixture without DCC1 proteins was used as the control 678

(left and middle lanes). C, Relative activity of mitochondrial respiratory complex I. Mitochondria 679

were isolated from calli (0.1 g) of wild type (Col-0), dcc1, ca2, and dcc1ca2 cultured on SIM at 16 680

days. 20 μg mitochondrial proteins were used to determine the Complex I activity. The absorbance 681

of all samples was measured at 340 nm for 60 min using a plate reader. Complex I activity was 682

calculated from the decrease in absorbance per minute. Functional loss of DCC1 or CA2 resulted in 683

the reduced activity of Complex I. D, Relative activity of complex I in calli of dcc1ca2 after 684

addition of recombinant CA2 or DCC1 proteins. Purified CA2-His proteins and DCC1-His proteins 685

were added to the assay mixture. Only both additions of DCC1 and CA2 proteins completely 686

rescued the reduced complex I activity. Significant difference, **p < 0.01 (Student’s one-tailed t 687

test). 688

Figure 6. Mutation of DCC1 or CA2 results in the increased ROS levels. A, Levels of ROS in calli 689

of Col-0, dcc1, ca2, and dcc1ca2 on CIM and SIM at indicated times by DAB staining. B, Relative 690

ROS staining intensity in calli of wild type (Col-0), dcc1, ca2, and dcc1ca2 on CIM and SIM at 691

indicated times. C3 and C6 indicate calli cultured on CIM at 3 and 6 days, respectively. S4, S8, S12 692



34

and S16 indicate calli cultured on SIM at 4, 8, 12 and 16 days, respectively. Standard errors were 693

calculated from three sets of biological replicates and more than 100 calli were examined in each 694

replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 (Student’s one-tailed t test). 695

Figure 7. Treatment with exogenous ROS inhibits shoot regeneration. A to C, Callus morphology 696

(A), frequencies of shoot regeneration from calli (B) and number of shoots per callus (C) in wild 697

type (Col-0) after treatment with H2O2 at different concentrations during shoot regeneration. S12, 698

S16, S20, S24 and S28 indicate calli cultured on SIM at 12, 16, 20, 24 and 28 days, respectively. 699

Standard errors were calculated from three sets of biological replicates and more than 100 calli were 700

examined in each replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 (Student’s 701

one-tailed t test). 702

Figure 8. Decreased ROS level rescues phenotypes of dcc1ca2 double mutant. A to C, Callus 703

morphology (A), frequencies of shoot regeneration from calli (B), and number of shoots per callus 704

(C) in wild type (Col-0), dcc1, ca2, and dcc1ca2 after treatment with GSH (600 μM) or 705

overexpression of CAT3 on SIM at 28 days. Glutathione (GSH) is a main endogenous antioxidant 706

responsible for ROS removal. CAT3 encodes a catalase, which catalyzes the breakdown of H2O2 707

into water and oxygen, thereby reducing the H2O2 level. pER8-CAT3 represents the over-expression 708

of CAT3 in dcc1, ca2, and dcc1ca2 background when induced with estradiol, respectively. Standard 709

errors were calculated from three sets of biological replicates and more than 100 calli were 710

examined in each replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 (Student’s 711

one-tailed t test). 712

Figure 9. Transcript levels of master genes involved in shoot regeneration. A and B, Transcript 713

levels of master genes for callus formation (A) and shoot meristem induction (B) during shoot 714

regeneration. C3 and C6 represent calli cultured on CIM at 3 and 6 days using roots as explants 715

before transfer to SIM. S4, S8, S12 and S16 indicate calli cultured on SIM at 4, 8, 12, 16 days, 716

respectively. Standard errors were calculated from three sets of biological replicates. Significant 717

difference, **p < 0.01 (Student’s one-tailed t test). 718

Figure 10. DCC1 regulates shoot regeneration through modulating multiple signaling by RNA-seq 719

analyses. A, Differential gene expression detected by edgeR. Two-fold change in gene transcript 720

levels between wild type Col-0 and mutant dcc1 with an adjusted P value (FDR) cutoff 0.05 was 721

considered as differential expression: 2332 genes were down-regulated and 689 genes were 722



35

up-regulated in dcc1 mutant. B, GO analyses of down-regulated genes in dcc1 mutant. C, Cluster 723

analysis of transcript levels of genes involved in auxin signaling, meristem initiation, and organ 724

formation. Col-0-A, Col-0-B, and Col-0-C were three repeats of Col-0. dcc1-A, dcc1-B, and dcc1-C 725

were three repeats of dcc1 mutant. D, Transcript levels of TAA1, YUC4, GH3.6, SAUR51, KNAT2, 726

CLV1, WOX1, and CUC1 in calli of Col-0, dcc1, and H2O2 (wild-type treated with 0.01‰ H2O2 727

during shoot regeneration) on SIM at 16 days, as determined by qRT-PCR. TUBULIN2 (TUB2) was 728

the reference gene. Significant difference, **p < 0.01 (Student’s one-tailed t test). E, Response 729

patterns of DR5rev:GFP in calli with or without H2O2 treatment on SIM at indicated times. S0, calli 730

cultured on CIM at 6 days using roots as explants before transfer to SIM. S4, S8, S12, S16, calli 731

cultured on SIM at 4, 8, 12 and 16 days, respectively. 732

Figure 11. DCC1 regulates the capacity of shoot regeneration among different Arabidopsis 733

ecotypes. A, Linkage disequilibrium analyses of DCC1 in 48 Arabidopsis ecotypes indicated five 734

critical SNPs (108, 147, 174, 175, 378, 481). B, Two haplotypes (Hap) of DCC1 was characterized 735

based on five SNPs of nucleotide sequences in Arabidopsis natural variants. C, Amino acid 736

sequence of Hap1 and Hap2. Two SNPs (SNP 175 and 481) resulted in amino acid mutation (I59V 737

and I161V). D and E, Shoot regeneration frequencies from calli (D) and number of shoots per callus 738

(E) in each haplotype group (n, number of genotypes belonging to each haplotype group). F, 739

Purified proteins were subjected to SDS-PAGE and stained by Coomassie Brilliant Blue R-250. 740

DCC1-WT from Col-0 was used as the control. DCC1-m175, DCC1-m481 and DCC1-m175/m481 741

were mutated according to Hap2 SNPs (SNP 175 and SNP 481). G, Insulin reduction assay by the 742

various proteins. Purified proteins were subjected to a reduction assay by using fluorescein 743

isothiocyanate-labeled insulin (FiTC-insulin) as the substrate, which displayed higher fluorescence 744

after disulfide reduction. The assay mixture lacking recombinant proteins served as the control. 745

Fluorescence intensity was recorded at 515-525 nm emission after 480-495 nm excitation for 120 746

minutes in a fluorescent plate reader at room temperature. H, Both SNP 175 and SNP 481 were 747

critical for interaction of DCC1 and CA2 by yeast two-hybrid assay. I, Frequencies of shoot 748

regeneration from calli of wild type (Col-0), dcc1, pDCC1:DCC1-dcc1, and 749

pDCC1:DCC1-m175-m481-dcc1 on SIM at 28 days. Significant difference, **p < 0.01; nsp > 0.05 750

(Student’s one-tailed t test). 751

Figure 12. ROS levels are associated with shoot regeneration capacity of different ecotypes in 752



36

Arabidopsis. A, DAB staining showing ROS levels in calli of different ecotypes of Hap1 cultured 753

on SIM at 16 days. B, DAB staining showing ROS levels in calli of different ecotypes of Hap2 754

cultured on SIM at 16 days. C, Shoot regeneration frequencies from calli of different ecotypes 755

cultured on SIM at 28 days. D, Number of shoots per callus of different ecotypes cultured on SIM at 756

28 days. E, Relative staining intensity of ROS in calli of different ecotypes cultured on SIM at 16 757

days. Standard errors were calculated from three sets of biological replicates and more than 100 758

calli were examined in each replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 759

(Student’s one-tailed t test). 760

761

762



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http://scholar.google.com/scholar?as_q=Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bashandy&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Balmer Y%2C Vensel WH%2C Tanaka CK%2C Hurkman WJ%2C Gelhaye E%2C Rouhier N%2C Jacquot J%2DP%2C Manieri W%2C Sch�rmann P%2C Droux M%2C et al %282004%29 Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria%2E Proc Natl Acad Sci USA 101%3A 2642%2D2647&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Benitez%2DAlfonso Y%2C Cilia M%2C San Roman A%2C Thomas C%2C Maule A%2C Hearn S%2C Jackson D %282009%29 Control of Arabidopsis meristem development by thioredoxin%2Ddependent regulation of intercellular transport%2E Proc Natl Acad Sci USA 106%3A 3615%2D3620&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106: 3615-3620

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http://www.ncbi.nlm.nih.gov/pubmed?term=Birnbaum KD%2C Alvarado AS %282008%29 Slicing across kingdoms%3A regeneration in plants and animals%2E Cell 132%3A 697%2D710&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697-710

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http://www.ncbi.nlm.nih.gov/pubmed?term=Viola IL%2C G�ttlein LN%2C Gonzalez DH %282013%29 Redox modulation of plant developmental regulators from the class I TCP transcription factor family%2E Plant Physiol 162%3A 1434%2D1447&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A Two-Step Model for de novo Activation of WUSCHEL during Plant Shoot Regeneration&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A Two-Step Model for de novo Activation of WUSCHEL during Plant Shoot Regeneration&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhao Y %282010%29 Auxin biosynthesis and its role in plant development%2E Annu Rev Plant Bio 61%3A 49%2D64&dopt=abstract


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Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH (2015) Arabidopsis CALCIUM-DEPENDENT PROTEINKINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under droughtstress. Plant Cell 27: 1445-1460



http://search.crossref.org/?page=1&rows=2&q=Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Bio 61: 49-64

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhao&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin biosynthesis and its role in plant development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin biosynthesis and its role in plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zou JJ%2C Li XD%2C Ratnasekera D%2C Wang C%2C Liu WX%2C Song LF%2C Zhang WZ%2C Wu WH %282015%29 Arabidopsis CALCIUM%2DDEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid%2Dmediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress%2E Plant Cell 27%3A 1445%2D1460&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH (2015) Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27: 1445-1460

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zou&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zou&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


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