Short title: SINE proteins function in stomatal dynamics · 127 conditions. On average, neither sine1-1 nor sine2-1 stomata were fully open or fully closed for 128 the duration of

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Short title: SINE proteins function in stomatal dynamics 1

2

Author for contact: Iris Meier 3

The Ohio State University, 520 Aronoff Laboratory, 4

Columbus, OH 43210 5

[email protected], (614) 292 8323 6

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Article Title: A role for plant KASH proteins in regulating stomatal dynamics 8

9

Alecia Biel1, Morgan Moser

1, and Iris Meier

1,2,* 10

11

1Department of Molecular Genetics, The Ohio State University, Columbus, OH, USA 12

2 Center for RNA Biology, The Ohio State University, Columbus, OH, USA 13

* Address correspondence to [email protected] 14

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One-sentence summary: Protein complexes at the nuclear envelope – known to connect the 16

nucleus to the cytoskeleton – play a role in stomatal opening and closing in response to a variety 17

of signals. 18

19

Author contributions: A.B. and I.M conceived and planned the experiments. A.B. performed and 20

analyzed most of the experiments. M.M. performed and analyzed the ROS experiment. A.B. and 21

I.M. and wrote the article with assistance by M.M. I.M. supervised the project and provided 22

funding. 23

24

The author responsible for distribution of materials integral to the findings presented in this 25

article in accordance with the policy described in the Instructions for Authors 26

(www.plantphysiol.org) is: Iris Meier ([email protected]) 27

28

Funding: This work was supported by a grant from the National Science Foundation to I.M. 29

(NSF-1613501). 30

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Plant Physiology Preview. Published on November 25, 2019, as DOI:10.1104/pp.19.01010

Copyright 2019 by the American Society of Plant Biologists

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2

Abstract 32

Stomatal movement, which regulates gas exchange in plants, is controlled by a variety of 33

environmental factors, including biotic and abiotic stresses. The stress hormone abscisic acid 34

(ABA) initiates a signaling cascade, which leads to increased H2O2 and Ca2+

levels and F-actin 35

reorganization, but the mechanism of, and connection between, these events is unclear. SINE1, 36

an outer nuclear envelope component of a plant Linker of Nucleoskeleton and Cytoskeleton 37

(LINC) complex, associates with F-actin and is, along with its putative paralog SINE2, expressed 38

in guard cells. Here, we have determined that Arabidopsis (Arabidopsis thaliana) SINE1 and 39

SINE2 play an important role in stomatal opening and closing. Loss of SINE1 or SINE2 results 40

in ABA hyposensitivity and impaired stomatal dynamics but does not affect stomatal closure 41

induced by the bacterial elicitor flg22. The ABA-induced stomatal closure phenotype is, in part, 42

attributed to impairments in Ca2+

and F-actin regulation. Together, the data suggest that SINE1 43

and SINE2 act downstream of ABA but upstream of Ca2+

and F-actin. While there is a large 44

degree of functional overlap between the two proteins, there are also critical differences. Our 45

study makes an unanticipated connection between stomatal regulation and nuclear envelope-46

associated proteins, and adds two new players to the increasingly complex system of guard cell 47

regulation. 48

49



3

Introduction 50

Eukaryotic nuclei are double membrane-bound organelles with distinct but continuous inner 51

nuclear membranes (INM) and outer nuclear membranes (ONM). The site where the INM and 52

ONM meet forms the nuclear pore, where nucleocytoplasmic transport occurs (Jevtić et al., 53

2014). Spanning the INM and the ONM are protein complexes known as linker of the 54

nucleoskeleton and cytoskeleton (LINC) complexes. LINC complexes contribute to nuclear 55

morphology, nuclear movement and positioning, chromatin organization and gene expression, 56

and have been connected to human diseases (Chang et al., 2015; Chang et al., 2015; Lv et al., 57

2015). LINC complexes are comprised of Klarsicht/ANC-1/Syne Homology (KASH) ONM 58

proteins and Sad1/UNC-84 (SUN) INM proteins that interact in the lumen of the nuclear 59

envelope (NE), thus forming a bridge between the nucleoplasm and the cytoplasm. 60

Opisthokonts (animals and fungi) and plants have homologous SUN proteins with C-terminal 61

SUN domains located in the NE lumen. However, no proteins with sequence similarity to animal 62

KASH proteins have been discovered in plants and thus much less is known regarding the 63

function of plant LINC complexes (Graumann et al., 2010; Oda and Fukuda, 2011). Within the 64

past few years, studies identifying structurally similar plant KASH protein analogs have 65

stimulated increased interest in this area (Zhou et al., 2012; Graumann et al., 2014; Zhou et al., 66

2014; Zhou et al., 2015). Arabidopsis (Arabidopsis thaliana) ONM-localized WPP domain-67

interacting proteins (WIPs) were the first identified plant analogs of animal KASH proteins, 68

binding the SUN domain of Arabidopsis SUN1 and SUN2 in the NE lumen (Zhou et al., 2012). 69

WIP1, WIP2, and WIP3 form a complex with WPP-interacting tail-anchored proteins (WIT1 and 70

WIT2). Together, they are involved in anchoring the Ran GTPase activating protein RanGAP to 71

the NE (Zhou et al., 2012), in nuclear movement in leaf mesophyll and epidermal cells and root 72

hairs (Zhou et al., 2012; Tamura et al., 2013; Zhou and Meier, 2013; Tamura et al., 2015), and in 73

nuclear movement in pollen tubes (Zhou et al., 2015). 74

Based on similarity to the SUN-interacting C-terminal tail domain of WIP1-WIP3, additional 75

plant-unique KASH proteins were identified and named SUN domain-interacting NE proteins 76

(SINE1-SINE4 in Arabidopsis) (Zhou et al., 2014). Arabidopsis SINE1 and SINE2 are putative 77

paralogs and are conserved among land plants (Poulet et al., 2017). In leaves, SINE1 is 78

exclusively expressed in guard cells and the guard cell developmental lineage, whereas SINE2 is 79



4

expressed in trichomes, epidermal and mesophyll cells, and only weakly in mature guard cells 80

(Zhou et al., 2014). Both SINE1 and SINE2 are also expressed in seedling roots and share an N-81

terminal domain with homology to armadillo (ARM). Proteins encoding ARM repeats have been 82

reported to bind actin and act as a protein-protein interaction domain in a multitude of proteins 83

across both plant and animal kingdoms (Coates, 2003). SINE1 was verified to associate with 84

filamentous actin (F-actin) via its ARM domain through colocalization studies in N. 85

benthamiana leaves and Arabidopsis roots, but SINE2 does not share this property (Zhou et al., 86

2014). Furthermore, depolymerization of F-actin by latrunculin B (LatB) disrupts GFP-SINE1 87

localization in guard cells and increases GFP-SINE1 mobility during FRAP analysis, suggesting 88

a SINE1-F-actin interaction in guard cells. Mutant analysis showed that SINE1 is required for 89

the symmetric, paired localization of nuclei in guard cells, while SINE2 contributes to plant 90

immunity against the oomycete pathogen Hyaloperonospora arabidopsis (Zhou et al., 2014). 91

Stomatal dynamics rely on highly coordinated and controlled influx and efflux of water and ions 92

which increase turgor pressure to facilitate opening and decrease turgor for stomatal closing. 93

This process is mediated through complex signal transduction pathways, being controlled by 94

plant and environmental parameters such as changes in light conditions and abiotic and biotic 95

stresses (Schroeder et al., 2001). Light changes result in a conditioned stomatal response in 96

which stomata open and close in a daily cyclic fashion. Abiotic stresses, such as drought, and 97

biotic stresses, such as pathogen exposure, can both override this daily cycle to induce a specific 98

stomatal response. 99

The plant hormone abscisic acid (ABA) senses and responds to abiotic stresses, with ABA 100

metabolic enzymes regulated by changes in drought, salinity, temperature, and light (Zhang et 101

al., 2008; Xi et al., 2010; Verma et al., 2016). ABA initiates long-term responses, such as growth 102

regulation, through alterations in gene expression (Kang et al., 2002; Fujita et al., 2005) and 103

induces stomatal closure as a short-term response to stress, involving the activation of guard cell 104

anion channels and cytoskeleton reorganization (Eun and Lee, 1997; Zhao et al., 2011; Jiang et 105

al., 2012; Li et al., 2014). F-actin is radially arrayed in open guard cells of several diverse plant 106

species and undergoes reorganization into a linear or diffuse bundled array upon stomatal closure 107

(Kim et al., 1995; Xiao et al., 2004; Li et al., 2014; Zhao et al., 2016). Although many disparate 108



5

players have been shown to be important for regulating stomatal dynamics, it is still unclear how 109

these events are interconnected and where actin reorganization fits in. 110

Here, we have investigated if Arabidopsis SINE1 and SINE2 play a physiological role in guard 111

cell biology. Our findings show that both SINE1 and SINE2 are involved in stomatal opening 112

and closing. Loss of SINE1 or SINE2 results in ABA hyposensitivity and impaired stomatal 113

dynamics but does not affect pathogen-induced stomatal closure from the bacterial peptide flg22. 114

The ABA-induced stomatal closure phenotype is, in part, attributed to impairments in Ca2+

and 115

actin regulation. 116

Results 117

SINE1 and SINE2 are involved in light regulation of stomatal opening and closing 118

To assess whether SINE1 and SINE2 have a function in guard cell dynamics, we first monitored 119

stomatal aperture changes in sine1-1, sine2-1, and sine1-1 sine2-1 mutants under short day 120

conditions (8h light, 16h dark) using in vivo stomatal imprints from attached leaves. Two hours 121

prior to light exposure, average stomatal apertures were between 2.8 and 3.3 µm (Fig. 1A). By 122

mid-day, after four hours of light exposure, WT stomata were fully opened, while sine1-1 and 123

sine2-1 stomata had only opened marginally, and sine1-1 sine 2-1 behaved more like WT (see 124

below). Expression of proSINE1:GFP-SINE1 in sine1-1 (SINE1:sine1-1) or proSINE2:GFP-125

SINE2 in sine2-1 (SINE2:sine2-1) partially restored stomatal responsiveness to changes in light 126

conditions. On average, neither sine1-1 nor sine2-1 stomata were fully open or fully closed for 127

the duration of the assay. 128

To further assess stomatal opening, detached leaves from WT and sine mutants (sine1-1, sine2-1, 129

and sine1-1 sine2-1) were incubated in buffers containing Ca2+

, K+, Ca

2+, and K

+, or neither ion 130

(Fig. 1B). Similar to methods described in Li et al. (2014) and Zhao et al. (2011), whole leaves 131

were incubated in specified buffer throughout the duration of the assay and epidermal peels were 132

taken and mounted just prior to imaging. In the absence of external K+ and Ca

2+ (opening buffer 133

(OB) base), light-induced stomatal opening was impaired in sine1-1, sine2-1, and sine1-1 sine2-1 134

(Fig. 1B, top left panel). With exposure to external Ca2+

, sine1-1, sine2-1, and sine1-1 sine2-1 135

still displayed significantly impaired stomatal opening (Fig. 1B, top right panel). Likewise, with 136



6

exposure to external K+, statistically significant impairment during opening was observed in both 137

single and double mutants (Fig. 1B, bottom left panel). Following exposure to both Ca2+

and K+, 138

stomatal opening in sine1-1 and sine2-1 was still somewhat reduced compared to WT (Fig. 1B, 139

bottom right panel), but less so than when one or both ions were missing. Similar positive effects 140

of low concentrations of Ca2+

on stomatal opening have been previously described (Hao et al., 141

2012; Wang et al., 2014). In all assays, SINE1:sine1-1 and SINE2:sine2-1 displayed similar 142

opening to WT, indicating full rescue of the mutant phenotypes. Finally, dark-induced stomatal 143

closure was assessed by comparing leaves transitioned from 3 hours of light to 3 hours of dark to 144

those kept under constant light. sine1-1, sine2-1, and sine1-1 sine2-1 were significantly impaired 145

in this closing response, suggesting that SINE1 and SINE2 are also required for dark-induced 146

stomatal closure (Fig. 1C). Together, these data indicate that SINE1 and SINE2 are involved in 147

stomatal opening in response to white light and closing in response to dark, and that exogenous 148

Ca2+

and K+

can at least partially rescue opening. 149

Impaired ABA-induced stomatal closure in sine1-1 and sine2-1 150

Abscisic acid (ABA) has been widely used to induce stomatal closure and monitor stomatal 151

response to simulated abiotic stress (Umezawa et al., 2010) and was used here to test ABA 152

stomatal response in sine mutants. Prior to this assay, we tested stomatal opening for all lines 153

used here to ensure equal starting conditions for the closing assays (Supplemental Fig. S1). 154

Stomatal closure in response to ABA was observed as early as one hour after exposure to 20 µM 155

ABA in all sine mutants when compared to WT (Fig. 2A). WT stomata continued to close over 156

the following two hours, while sine1-1 (Fig. 2A, left panel), sine2-1 (Fig. 2A, right panel), and 157

sine1-1 sine2-1 (Fig. 2A left and right panel) did not exhibit further stomatal closure 158

(representative images for WT and sine1-1 shown in Fig. 2B). In this assay, sine1-1 sine2-1 159

stomatal closure resembled that of sine1-1 and sine2-1 single mutants. This suggests that there is 160

no additive effect of the sine1-1 and sine2-1 mutants in this response, indicating SINE1 and 161

SINE2 are working in the same pathway. 162

Exogenous ABA induced stomatal closure in SINE1:sine1-1 and SINE2:sine2-1 at a similar rate 163

to WT (Fig. 2A). To determine if both SINE1 and SINE2 are independently required in ABA-164

induced stomatal closure, the following partially complemented lines were used: SINE1pro:GFP-165



7

SINE1 in sine1-1 sine2-1 (SINE1:sine1-1 sine2-1), and SINE2pro:GFP-SINE2 in sine1-1 sine2-166

1 (SINE2:sine1-1 sine2-1) (Zhou et al., 2014). Upon ABA exposure, SINE1:sine1-1 sine2-1 and 167

SINE2:sine1-1 sine2-1 showed significantly impaired stomatal closure compared to WT. Hence, 168

neither SINE1 nor SINE2 alone is sufficient to rescue the sine1-1 sine2-1 phenotype, confirming 169

that both proteins are independently required for this process. 170

To confirm the mutant phenotypes for additional alleles, the T-DNA insertion mutants sine1-3 171

and sine2-2 were used and compared to the SINE1:sine1-3 and SINE2:sine2-2 complemented 172

lines and the partially complemented lines SINE1:sine1-3 sine2-2 and SINE2:sine1-3 sine2-2 173

(Zhou et al., 2014). Similar results were obtained for an ABA-induced stomatal closure assay, 174

confirming independence of the phenotypes from insertion position and genetic background 175

(Supplemental Fig. S2). Therefore, only the sine1-1 and sine2-1 alleles were used for the 176

subsequent assays. 177

In addition to inducing stomatal closure, ABA also inhibits stomatal opening (Yin et al., 2013). 178

To test the role of SINE1 and SINE2 in this process, stomatal opening assays utilizing OB were 179

performed in the presence of 20 µM ABA (Fig. 2C). Under these conditions, WT, SINE1:sine1-180

1, and SINE2:sine2-1 are unable to open stomata in the presence of ABA. However, sine1-1, 181

sine2-1, and sine1-1 sine2-1 stomata are unimpeded in their ability to open, indicating loss of 182

SINE1 or SINE2 results in hyposensitivity to ABA for both opening and closing. 183

Stomatal closure can also be induced by biotic stresses, such as pathogen exposure (Zhang et al., 184

2008; Guzel Deger et al., 2015). The bacterial elicitor flg22 is a well-studied and accepted tool to 185

simulate pathogen-induced stomatal closure, and was therefore tested here. As a control, we used 186

the LRR receptor-like kinase mutant fls2-1, which is unable to recognize and bind flg22 187

(Dunning et al., 2007). After exposure to 5 µM flg22, fls2-1 had significantly inhibited stomatal 188

closure compared to WT, while flg22-induced stomatal closure in sine1-1 and sine2-1 was 189

similar to that of WT (Fig. 2D). Together, these data indicate that SINE1 and SINE2 are working 190

within the ABA pathway to regulate ABA-induced stomatal closure and ABA-inhibition of 191

stomatal opening and that these roles are distinct from the flg22-induced stomatal closure 192

pathway. 193

Drought susceptibility is increased in sine1-1 and sine2-1 plants after stomatal opening 194



8

If stomata are unable to close in response to stress, an increase in transpiration is expected (Kang 195

et al., 2002; Mustilli et al., 2002). To test this for sine mutants, leaves detached at midday were 196

kept in a petri dish and weighed collectively for each genotype. Fresh weight loss was similar in 197

sine2-1, sine1-1 sine2-1, SINE1:sine1-1, and SINE2:sine2-1 compared to WT (Fig. 3A). 198

Although sine1-1 did show a statistically significant increase in fresh weight loss compared to 199

WT (P<0.05), there was no difference observed between sine1-1 and SINE1:sine1-1. Thus, there 200

appears to be no conclusive difference in fresh weight loss between WT, sine1-1, and sine2-1. To 201

test if this is due to the fact that sine1-1 and sine2-1 were impaired both in opening and closing, 202

we repeated the water loss assay with leaves first incubated for 3 hours in OB. As a control, 203

detached leaves were exposed to OB base (without Ca2+

or K+, Fig. 3B). In this case, similar 204

results were obtained as in the air-only treatment. However, after pre-exposure to OB, sine1-1 205

and sine2-1 leaves lost weight at a significantly faster rate than WT, while SINE1:sine1-1 and 206

SINE2:sine2-1 lost weight at similar rates as WT. Conversely, sine1-1 sine2-1 showed an 207

intermediate phenotype with no statistically significant difference to WT (Fig. 3C, P<0.05). Leaf 208

morphology of sine1-1 and sine2-1 agreed with these observations in that pre-exposure to OB led 209

to more rapid wilting, as seen by increased leaf curling and shrinking compared to WT (Fig. 3D). 210

In a second experimental setting, individual leaves were placed abaxial side up throughout the 211

assay and weighed separately to avoid a potential influence of overlapping leaves (Supplemental 212

Fig. S3A-B). Also, an additional T-DNA allele combination for the double mutant (sine1-3 213

sine2-2) was added to exclude potential influence of the genetic background. In addition, two 214

lines expressing SINE1 and SINE2 under control of the 35S promoter in a WT background were 215

added: 35S:GFP-SINE1 in WT (SINE1:WT) and 35S:GFP-SINE1 in WT (SINE2:WT). These 216

data largely recapitulated those shown in Figure 3, suggesting that different incubation 217

conditions did not influence the assay. Both double mutants lost water at an intermediate rate 218

compared to WT and the single mutants (Supplemental Fig. S3C), again consistent with the leaf 219

morphology at the end of the assay (Supplemental Fig. S3B). Together, this suggests that the 220

combination of an opening and closing defect masks any transpiration phenotype. Thus, induced 221

stomatal opening reveals increased drought susceptibility in sine1-1, sine2-1, and partially in 222

sine1-1 sine2-1. 223

Mapping the position of SINE1 and SINE2 in the stomatal ABA signaling pathway 224



9

Upon ABA perception, a signaling cascade results in the induction of both H2O2 and Ca2+

(Pei et 225

al., 2000; Umezawa et al., 2010; Zhao et al., 2011). To narrow down the position of SINE1 and 226

SINE2 in the ABA-induced stomatal closure pathway, we investigated H2O2-induced and Ca2+

-227

induced stomatal closure. Stomatal closure was measured as described above, in response to 228

either 0.5 mM H2O2 or 2 mM CaCl2 (Zhao et al., 2011). Upon exposure to H2O2, stomatal 229

closure was impaired in sine1-1, sine2-1, and sine1-1 sine2-1 compared to WT (Fig. 4A, 4B). 230

SINE1:sine1-1 and SINE2:sine2-1 displayed H2O2 -induced stomatal closure similar to WT (Fig. 231

4A, 4B). Significantly reduced stomatal closure was seen in SINE1:sine1-1 sine2-1 and 232

SINE2:sine1-1 sine2-1, again confirming the single and double mutant results (Fig. 4A, 4B). 233

When exposed to CaCl2, sine1-1, sine2-1, and sine1-1 sine2-1 were somewhat impaired in 234

stomatal closure, which was also observed in the double mutant (Fig. 4C, 4D). However, 2 mM 235

CaCl2 more effectively triggered stomatal closure in sine1-1, sine2-1, and sine1-1 sine2-1 than 236

the previous treatments of ABA or H2O2 (Supplemental Table S1). Meanwhile, SINE1:sine1-1 237

and SINE2:sine2-1 lines showed stomatal closure similar to WT in response to exogenous 238

application of Ca2+

and SINE1:sine1-1 sine2-1 and SINE2:sine1-1 sine2-1 had a similar degree 239

of stomatal closure as single and double sine mutants (Fig. 4C, 4D). These results indicate that 240

external Ca2+

is able to partially rescue the stomatal closure phenotype. 241

Within the ABA pathway, there is feedback between the Ca2+

and H2O2 branches (Pei et al., 242

2000; Desikan et al., 2004; Zou et al., 2015). Thus, we also tested the stomatal response of sine1-243

1 and sine2-1 to a combination of both inducers. With exposure to both Ca2+

and H2O2, stomatal 244

closure was similar between sine2-1, sine1-1 sine2-1, WT, SINE1:sine1-1, and SINE2:sine2-1 245

(Fig. 4E). Finally, stomatal closure based on ABA, H2O2, Ca2+

, and darkness was expressed as 246

percentage of the aperture size at the beginning of the assay (Supplemental Table S2; see 247

Materials and Methods). This did not lead to any change in the data interpretation described 248

above. Together, these data show that the impaired stomatal closure response of SINE1 and 249

SINE2 mutants can be partially rescued by external Ca2+

, but not by H2O2. 250

Stomatal overexpression of SINE2 leads to compromised stomatal dynamics 251

SINE1 and SINE2 expression patterns differ with regards to guard cells and epidermal cells. 252

Thus, we assessed the impact of their ubiquitous expression on stomatal dynamics. 35S:GFP-253



10

SINE1 in WT (SINE1:WT) and 35S:GFP-SINE2 in WT (SINE2:WT), respectively, were 254

compared to SINE1pro:GFP-SINE1 (SINE1:sine1-1) and SINE2pro:GFP-SINE2 (SINE2:sine2-255

1). Confocal microscopy showed that SINE1:WT and SINE1:sine1-1 have similar expression 256

levels in guard cells (Fig. 5A, 5B). However, as expected, SINE2:WT showed significantly 257

higher GFP expression in guard cells than SINE2:sine2-1. Indeed, under the assay conditions, no 258

GFP signal above background was detected in SINE2:sine2-1-expressing guard cells (Fig. 5A, 259

5B). In contrast, immunoblots of protein extracts from whole seedlings and rosette leaves of 260

SINE1:WT, SINE2:WT, SINE1:sine1-1, and SINE2:sine2-1 showed similar amounts of GFP 261

fusion protein (Supplemental Fig. S4). This confirms that GFP-SINE2 is expressed in 262

SINE2:sine2-1 and indicates that SINE2:WT leads to overexpression of GFP-SINE2 in guard 263

cells compared to the native SINE2 promoter. 264

Next, we tested stomatal impairment in the SINE1 and SINE2 ubiquitously expressing lines. 265

While SINE1:WT behaved like WT, SINE2:WT recapitulated the sine1-1 phenotype during a 266

light/dark cycle (Fig. 5C). Similarly, SINE2:WT was largely unresponsive to ABA, while 267

SINE1:WT showed WT-like stomatal closure (Fig. 5D). Thus, 35S promoter-driven GFP-SINE1 268

expression has no significant effect on SINE1/SINE2 function in guard cells. However, 269

additional expression of the normally lowly expressed SINE2 in guard cells appears toxic to 270

SINE1/SINE2 function. This suggests that fine-tuning of cellular abundance of the two proteins 271

is required for their function. Because one model to account for the interference of SINE2 is that 272

accumulation of a SINE1/SINE2 heterodimer could negatively affect a specific role of SINE1 in 273

guard cells, we tested if the two proteins can interact in a split-ubiquitin yeast two-hybrid assay. 274

Indeed, interaction was seen between SINE1 and SINE2 as well as a weak interaction between 275

SINE2 and SINE2. Because of self-activation issues, the SINE1-SINE1 interaction could not be 276

tested (Supplemental Fig. S5). 277

Although SINE2:WT recapitulates the sine1-1 and sine2-1 phenotype in both a light/dark cycle 278

and in ABA response, this line showed WT-like loss of fresh weight during desiccation 279

(Supplemental Fig. S3). This could be explained if SINE2:WT had a compensatory phenotype, 280

such as altered stomatal density. SINE2 is normally expressed only in mature guard cells, 281

whereas SINE1 is expressed in both progenitor guard cells and mature guard cells (Zhou et al., 282

2014). We therefore tested if 35S promoter-driven SINE2 is also influencing stomatal 283



11

development (Lucas et al., 2006; Nadeau and Sack, 2002). Indeed, both stomatal index (SI) and 284

stomatal density (SD) are reduced in SINE2:WT, but not in SINE1:WT, WT, or the T-DNA 285

insertion mutants, suggesting that a compensatory phenotype might indeed exist (Supplemental 286

Fig S6). 287

Together, these data show that ubiquitous expression of SINE2 impairs stomatal response to 288

changes in light conditions as well as during ABA-induced stomatal closure. Additionally, 289

ubiquitous SINE2 expression resulted in altered stomatal development. These data suggest that 290

the abundance of SINE2 in guard cells might be tightly controlled and linked to SINE1/2 291

function. 292

Interactions between sine1-1 and sine2-1 mutants and the actin cytoskeleton 293

F-actin rearrangement has been implicated in stomatal dynamics and undergoes a specific pattern 294

of reorganization (Staiger et al., 2009). When this actin rearrangement is disrupted, there are 295

concomitant perturbations in stomatal dynamics (Kim et al., 1995; Xiao et al., 2004; Jiang et al., 296

2012; Li et al., 2014; Zhao et al., 2016). We tested here if the characterized sine mutants showed 297

interactions with drug-induced F-actin depolymerization or with F-actin stabilization during 298

stomatal closing. Latrunculin B (LatB) results in F-actin depolymerization and facilitates 299

stomatal closure in the presence of ABA (MacRobbie and Kurup, 2007). In contrast, 300

jasplakinolide (JK) stabilizes and polymerizes F-actin, inhibiting stomatal closure (MacRobbie 301

and Kurup, 2007; Li et al., 2014). We used LatB and JK in the presence and absence of ABA to 302

assess their influence on stomatal closure in sine1-1 and sine2-1. 303

When WT leaves are incubated in either OB or OB + LatB in the light, stomatal apertures 304

remained open during the three-hour assay (Fig. 6A). Similarly, both OB and OB + LatB 305

treatment of sine1-1 and sine2-1 resulted in open stomata throughout the assay (Fig. 6A). ABA 306

alone and ABA + LatB induced stomatal closure in WT, as reported previously (MacRobbie and 307

Kurup, 2007; Fig. 6A). ABA exposure in sine1-1 and sine2-1 resulted in minimal closure, as 308

shown above. However, treatment with ABA and LatB resulted in significant closure of stomata 309

in both sine1-1 (Fig. 6A, left panel P<0.001) and sine2-1 (Fig. 6A, right panel P<0.001), closely 310

resembling WT. This suggests that LatB treatment overcomes the inhibition of stomatal closure 311

caused by the loss of either SINE1 or SINE2. 312



12

Both under OB and OB + JK, stomata remained open in WT (Fig. 6B). JK inhibited ABA-313

induced closure in WT, as previously reported, indicating that actin depolymerization is 314

necessary for ABA-induced stomatal closure (MacRobbie and Kurup, 2007; Li et al., 2014). OB 315

alone resulted in sustained stomatal opening in sine1-1 mutants. JK treatment in the absence of 316

ABA led to stomatal closure in sine1-1 mutants, as did the combination of JK and ABA (Fig. 6B, 317

left panel). In contrast, JK did not induce stomatal closure in sine2-1 and did not rescue the 318

sine2-1 defect in ABA-induced stomatal closure (Fig. 5A, right panel). To account for any 319

differences seen in starting aperture size, the percent of stomatal closure was calculated 320

(Supplemental Table S3) and the results are similar to those described above. 321

Together, these data indicate that actin depolymerization rescues the defect in ABA-induced 322

stomatal closure that is caused by the loss of SINE1 or SINE2, and that in the absence of SINE1, 323

JK-induced actin stabilization and polymerization can mimic the effect of ABA. 324

Discussion 325

We have shown here that two related plant KASH proteins, SINE1 and SINE2, play similar, yet 326

distinguishable, roles in stomatal dynamics in response to light, dark, and ABA. We have 327

previously reported that, in leaves, SINE1 is expressed in guard cells and the guard cell 328

developmental lineage, while SINE2 is expressed predominantly in leaf epidermal and 329

mesophyll cells, and only weakly detected in mature guard cells (Zhou et al., 2014). GFP fusion 330

proteins of SINE1 and SINE2 decorate the nuclear envelope, as expected based on their KASH-331

protein function, but SINE1 is also localized in a filamentous pattern that resembles actin in 332

guard cells and mature root cells, and this localization can be abolished by actin-depolymerizing 333

drugs (Zhou et al., 2014). In sine1 mutant lines it was observed that the guard cell nuclei, which 334

are typically arranged opposite each other in the center of the paired guard cells, are shifted from 335

this position. This cellular phenotype was recapitulated in LatB-treated wild-type guard cells, 336

suggesting actin involvement, but no effect was found in sine2 mutants. Based on these cell 337

biological data, we hypothesized a function for SINE1, but not necessarily for SINE2, in guard 338

cell biology. 339

Interestingly, in most bioassays applied here, sine1 and sine2 mutants showed similar guard cell-340

related phenotypes, which were also recapitulated by the double mutant, suggesting that the two 341



13

proteins act in a shared pathway required for wild-type-like guard cell function. Loss of either 342

SINE1 or SINE2 greatly diminishes stomatal opening in response to light, as well as stomatal 343

closing in response to dark or ABA and significantly reduces the dynamic range of stomatal 344

apertures between night and midday (Figs. 1 and 2). The lack of responsiveness to light for 345

stomatal opening could be compensated in both single and double mutants through addition of 346

external potassium and a low concentration of Ca2+

. Both ions have been shown to play roles 347

during light-induced stomatal opening (Hao et al., 2012; Wang et al., 2014), thus suggesting that 348

the mutants might be hyposensitive to the external application of these ions (Fig. 1B). 349

During stomatal closure, ABA acts through Ca2+

-dependent and Ca2+

-independent signaling 350

events (Wang et al., 2013). ABA increases both the Ca2+

entry at the plasma membrane and the 351

internal Ca2+

release resulting in Ca2+

oscillations (Gilroy et al., 1991; Allen et al., 1999; Grabov 352

and Blatt, 1999; Hamilton et al., 2000; Schroeder et al., 2001; Jiang et al., 2014; An et al., 2016). 353

The increase in cellular Ca2+

is connected to reactive oxygen species (ROS) (Kwak et al., 2003; 354

Ogasawara et al., 2008) and ultimately results in the activation of K+ outward channels and slow 355

and fast ion channels (SLAC/ALMT), as well as the inactivation of K+ inward channels such as 356

KAT1 (Jezek and Blatt, 2017). We therefore tested if application of the ROS H2O2 and/or Ca2+

357

could rescue the sine mutant stomatal closure phenotype. While H2O2 alone had no or a minimal 358

effect, Ca2+

partially rescued the impaired stomatal closure phenotype and the combination of 359

Ca2+

and ROS rescued the sine mutants to WT levels of closure (Fig. 4). Consistent with this 360

finding, internal ROS increased after ABA exposure in sine1-1 and sine2-1 (Supplemental Fig. 361

S7A and S7B). In contrast, Fura-2 staining suggests that early cytoplasmic Ca2+

fluctuations after 362

exposure to ABA are dampened in sine1-1 and sine2-1, although it is important to note that all 363

Fura-2 data must take into account possible signal degradation due to any uncleared AM ester 364

(Supplemental Fig. 7C, 7D and 7E) (Kanchiswamy et al., 2014). Together, this suggests that, 365

within ABA signaling, SINE1 and SINE2 act upstream of Ca2+

, and that ROS exposure might 366

intensify the Ca2+

-based rescue, potentially through the described effect of ROS on activating the 367

Ca2+

channels (Kwak et al., 2003; Wang et al., 2013; Jezek and Blatt, 2017). 368

Mutants with defects in stomatal regulation often show drought susceptibility phenotypes, due to 369

their inability to fully close stomata and thus lose an excess of water through evaporation (Kang 370

et al., 2002; Zhao et al., 2016). However, when detached sine single and double mutant rosette 371



14

leaves were exposed to room air and monitored for fresh weight loss, no difference from wild-372

type leaves was observed (Fig. 3A). In light of the results of the light/dark assay (Fig. 1A) as 373

well as the impairment in both light-induced opening and ABA- or dark-induced closing of 374

stomata (Figs. 1B, 1C, and 2A), we reasoned that mutant plants and detached mutant leaves 375

might be less subject to evaporation because, on average, stomata neither fully open nor fully 376

close. This was substantiated by testing evaporation sensitivity after fully opening stomata by 377

incubation in opening buffer. Under these conditions, mutant leaves wilted more rapidly, 378

consistent with the observed defects in stomatal closure (Fig. 3). 379

When two lines that constitutively express SINE1 or SINE2 under control of the 35S promoter 380

were added to this assay (Supplemental Fig. S3), both lines showed a fresh weight loss 381

indistinguishable from wild-type plants. This is not surprising in case of SINE1, given that this 382

line showed no stomatal defects. Constitutive expression of SINE2, however, led to defects both 383

in the light/dark assay and during ABA-induced stomatal closure (Fig. 5C and D) that would be 384

consistent with a sine mutant-like hypersensitivity to evaporation. To assess whether constitutive 385

expression of SINE2 leads to additional - possibly compensatory - phenotypes, we calculated 386

stomatal density and stomatal index of fully developed rosette leaves (Supplemental Fig. S6). 387

Indeed, constitutive SINE2 expression leads to a reduction of both stomatal density and stomatal 388

index. No such reduction was observed in any other line tested (Supplemental Fig. S6). The 389

reduced number of stomata caused by constitutive SINE2 expression might thus compensate for 390

the closing defects in this line, and result in wild-type-like evaporation within the level of 391

resolution of our assay. Notably, this additional phenotype suggests that the SINE gene family 392

not only acts in stomatal function but might also play a role during stomatal development. Only 393

SINE1 is expressed throughout the guard cell developmental lineage, and mis-expression of 394

SINE2 might thus highlight a yet unexplored role for SINE1 in the guard cell developmental 395

program. 396

It was noted that the sine1-1 sine2-1 stomata respond differently from the sine1-1 and sine2-1 397

single mutants in the light/dark assay (Fig. 1A), but not in any of the subsequent assays. One 398

notable difference between the light/dark assay and all other assays is that the former was 399

performed on potted plants, using leaf imprints, while all other assays used detached leaves 400

during treatments and epidermal peels for imaging. We thus argued that a whole plant phenotype 401



15

might exist specifically in the double mutant that compensates for any stomatal dynamic defects 402

seen in the light/dark assay. As SINE1 and SINE2 are highly expressed in the seedling root 403

(Zhou et al., 2014), we investigated primary root (PR) and lateral root (LR) characteristics 404

(Supplemental Fig. S8). Of the four parameters tested, three showed significant differences in 405

only the sine1-1 sine2-1 double mutant: decreased PR length, number of LR, and LR density. No 406

differences were observed in LR length. While it is currently unknown if this root morphology 407

phenotype accounts for the behavior of the sine1-1 sine2-1 mutant in the light/dark assay, these 408

data demonstrate that the possibility of additional phenotypes unique to the double mutant have 409

to be taken into account when interpreting these data. 410

Considerably less is known about the signal transduction pathway that triggers stomatal closure 411

after exposure to dark. It is generally assumed, however, that many steps are shared with the 412

ABA pathway (Jezek and Blatt, 2017). For example, mutants in the PYR/PYL/RCAR ABA 413

receptors are also deficient in their stomatal response to darkness (Merilo et al., 2013). Similarly, 414

diurnal rhythmicity is closely linked to the increase of guard cell ABA during the night - based 415

both on de novo synthesis and import from the apoplast - and depletion of ABA levels during the 416

day (Daszkowska-Golec and Szarejko, 2013). Together, these known connections are consistent 417

with the sine mutant phenotypes observed here, and suggest a primary role for SINE1 and SINE2 418

in a step downstream of ABA, but upstream of Ca2+

. 419

There is a plethora of known effects of actin dynamics on stomatal aperture regulation (Kim et 420

al.,1995; Gao et al., 2008; Gao et al., 2009; Higaki et al. 2010; Eun et al., 2001; MacRobbie and 421

Kurup, 2007; Lemichez et al., 2001; Jiang et al., 2012; Li et al., 2014; Zhao et al., 2011). 422

Together with SINE1 association with F-actin in guard cells, this made us speculate whether the 423

sine mutant phenotypes are related to disturbances in guard cell actin dynamics. It has been 424

shown previously that the inhibitor of F-actin assembly LatB and the F-actin stabilizer JK have 425

opposite effects on ABA-based stomatal closure (MacRobbie and Kurup, 2007). While LatB 426

mildly enhanced closure in the presence of ABA, JK inhibited it. Our data recapitulate in 427

Arabidopsis these effects reported for Commelina communis (MacRobbie and Kurup, 2007). 428

Both sine1 and sine2 mutant phenotypes showed a clear interaction with the actin drugs. While 429

loss of either SINE1 or SINE2 inhibited ABA-induced closure, co-incubation with LatB rescued 430

this inhibition to a significant degree (Fig. 6A). A hypothesis consistent with this finding is that 431



16

SINE1 and SINE2 are connected to actin turnover during the transition from radial to 432

longitudinal arrays that accompanies stomatal closure. In the presence of LatB, this activity 433

would not be required. JK inhibited guard cell closure in both wild type and the sine2-1 mutant, 434

consistent with the assumption that actin de-polymerization is a required step. Surprisingly, JK 435

alone, in the absence of ABA, was able to trigger stomatal closure in the sine1-1 mutant (Fig. 436

6B). SINE1 might be required for an additional step involved in stabilizing F-actin, downstream 437

of ABA, and this step might be also required for closing. In wild-type guard cells, this could be 438

accomplished through ABA-triggered involvement of SINE1, and JK has therefore no further 439

effect. However, this step could be inhibited in the absence of SINE1, and could thus be rescued 440

by JK alone, mimicking the ABA response. More studies will be required to verify these 441

proposed actin-related functionalities of the two proteins, but the data already show (1) that there 442

is indeed an interaction between SINE1/2 function and actin worthy of further investigation, and 443

(2) that while SINE1 and SINE2 have many overlapping functions, there are also critical 444

differences, as revealed by the JK data. Future studies will have to focus on the real-time analysis 445

of actin dynamics in the different mutant backgrounds and under the different treatments and the 446

investigation of genetic interactions between sine mutants and the reported mutants of actin-447

modulating proteins involved in guard cell regulation. 448

In addition, it is possible that SINE1 and SINE2 influence vacuolar dynamics and/or vesical 449

trafficking. It has been shown that over 90% of solutes released from guard cells originate from 450

vacuoles. F-actin binds to vacuolar ion channels, where it, together with cytoplasmic Ca2+

, 451

regulates vacuolar K+ release during ABA-induced stomatal closure (MacRobbie and Kurup, 452

2007; Kim et al., 2010). Furthermore, several studies have noted the involvement of actin in 453

vesicle trafficking, in particular the transport and activation of the K+ channel KAT1 in response 454

to ABA (Leyman et al., 1999; Sutter et al., 2006; Sutter et al., 2007; Sokolovski et al., 2008; 455

Eisenach et al., 2012). 456

Together, we have shown that the two plant KASH proteins SINE1 and SINE2 function in 457

stomatal aperture regulation in a variety of scenarios that involve light, dark, and ABA. We 458

propose that they act downstream of ABA, and upstream of Ca2+

and actin. While there is a large 459

degree of functional overlap between the two proteins, there are also critical differences, and 460

their further analysis might shed light on the role of their intriguingly different expression 461



17

patterns. This study reveals an unanticipated connection between stomatal regulation and a class 462

of nuclear envelope proteins known to be involved in nuclear anchoring and positioning, and 463

adds two new players to the ever more complex world of guard cell biology (Albert et al., 2017). 464

Addressing the connection between the phenotypes described here and the cellular role of SINE1 465

in guard cell nuclear positioning will likely be one of the more groundbreaking avenues of 466

further study. 467

Materials and methods 468

Plant material 469

Arabidopsis (Arabidopsis thaliana) (ecotype Col-0) was grown at 25°C in soil under 8-h light 470

and 16-h dark conditions. For all assays, leaves were collected from 6-8 week-old Arabidopsis 471

plants grown under these conditions. The fls2-1 mutant has been reported previously (Uddin et 472

al., 2017). sine1-1 (SALK_018239C), sine2-1 (CS801355), and sine2-2 (CS1006876) were 473

obtained from the Arabidopsis Biological Resource Center while sine1-3 (GK-485E08-019738) 474

was obtained from GABI-Kat. All SINE1 and SINE2 lines used here were previously reported 475

(Zhou et al., 2014). 476

Stomatal aperture measurements 477

Stomatal bioassays were performed by detaching the youngest, fully expanded rosette leaves of 478

6- to 8-week-old plants grown under short-day conditions (8 hours light; 16 hours dark). 479

For the light/dark assay, Duro super glue (Duro, item #1400336) was applied to a glass slide and 480

the abaxial side of a leaf was pressed into the glue to create an imprint. Imprints were taken two 481

hours prior to the chamber lights turning on and every two hours until two hours after the lights 482

were turned off. The imprints were allowed to dry and subsequently imaged to obtain stomatal 483

aperture measurements. 484

All other stomatal assays involved placing leaves in a petri dish abaxial side up with opening 485

buffer (OB) containing 10 mM MES, 20 µM CaCl2, 50 mM KCl, and 1% (w/v) sucrose at pH 486

6.15 for 3 h under constant light, while leaves remained whole until designated time points at 487

which abaxial epidermal strips were carefully peeled and imaged using a confocal microscope 488



18

(Zhao et al., 2011; Li et al., 2014; Eclipse C90i; Nikon). While immediately peeling and 489

mounting may lead to small variations in starting aperture size between experiments, stomata 490

prepared in this way display opening and closing comparable to published fluctuations (Zhao et 491

al., 2011; Li et al., 2014). For some of the experiments, OB base containing 10 mM MES and 1% 492

(w/v) sucrose at pH 6.15 was used to test stomatal dynamics with and without addition of 20 µM 493

CaCl2 and/or 50 mM KCl. Stomatal closing assays were performed immediately after the 494

opening assays, in which leaves were transferred to closing buffer containing 10 mM MES at pH 495

6.15 with or without the following treatments, as indicated: 20 µM ABA, 2 mM CaCl2, 0.5 mM 496

H2O2, or 5 µM flg22 (Kang et al., 2002; Zhang et al., 2008b; Zhao et al., 2011). Leaves were 497

placed in darkness to induce stomatal closure for 3 h when mentioned. NIS-Elements software 498

was used for stomatal aperture measurements. 499

Transpiration assay 500

To monitor water loss, five to six fully expanded leaves were detached from each plant at similar 501

developmental stages (sixth to ninth true rosette leaves). For the “air only” assay, leaves were 502

placed adaxial side up in an open petri dish under constant light on a laboratory bench and leaf 503

weights were recorded every 30 minutes (Kang et al., 2002). For all other assays in Fig. 2, leaves 504

were placed adaxial side up in either OB, OB base, OB base with 20 µM CaCl2, or OB base with 505

50 mM KCl for 3 h to induce opening. Leaves were then dried briefly on Kimwipes (Kimberly-506

Clark, item# 34120) and placed adaxial side up in dry petri dishes for an additional 3 h under 507

constant light. Leaf weights were recorded every 30 minutes. For the transpiration assay in 508

Supplemental Fig. S2, leaves were placed abaxial side up in OB and then kept abaxial side up 509

throughout the duration of the assay on paper towels. Leaves were weighed individually. 510

Confocal microscopy and fluorescence intensity measurements 511

For the imaging and quantification shown in Figs. 5A and 5B, 6- to 8-week-old Arabidopsis 512

leaves were imaged using a confocal microscope (Eclipse C90i; Nikon). Image settings were 513

established first for the highest expressing line (35S:GFP-SINE1 in WT) to obtain a clearly 514

visible, but not overexposed, GFP fluorescence signal at the nuclear envelope. These settings 515

were then applied for imaging all other samples: a medium pinhole with a gain setting of 7.35 516

and the 488-nm laser set at 15% power. All images were taken at room temperature with a Plan 517



19

Flour 40x oil objective (numerical aperture of 1.3, Nikon). NIS-Elements software was used to 518

quantify fluorescence by drawing a region of interest around individual guard cell nuclei. 519

ROS and calcium production assays 520

Detection of ROS in stomata was performed as described previously (Li et al. 2014). Whole 521

leaves were incubated in OB adaxial side up for 3 h under constant light. Leaves with open 522

stomata were incubated in MES buffer pH 6.15 containing 50 µM of H2DCF-DA in the dark for 523

15 min and then washed with water. The leaves were then transferred to CB containing 20 µM 524

ABA for 15, 30, 60, or 120 min. At the indicated time points, abaxial epidermal strips were 525

peeled from the leaves for ROS detection by confocal microscopy with a setting of 488 nm 526

excitation and 525 nm emission. The experiments were repeated four times with at least 70 527

stomata for each time point. 528

Detection of Ca2+

in stomata was performed using the Fura-2 AM dye (Sigma Aldrich, CAS 529

108964-32-5) (Jiang et al., 2014). Epidermal peels were floated in 10 mM MES-TRIS (pH 6.1) 530

buffer containing 1 µM Fura-2 AM and kept at 4°C in the dark for two hours. The Fura-2 dye 531

was then washed out and peels were placed back in opening buffer for one hour at RT. ABA was 532

added and time-lapse imaging of stomata was performed using confocal microscopy at specified 533

time intervals. Z-stacks of stomata were taken at each time point and mean intensity projections 534

were used for quantification. NIS-Elements was used to isolate and quantify cytoplasmic 535

fluorescence in order to exclude chloroplast signals. 536

Immunoblotting 537

N. benthamiana leaves were collected and ground in liquid nitrogen into powder, and protein 538

extractions were performed at 4°C. 1 ml radioimmunoprecipitation (RIPA) buffer was used to 539

extract 500 μl of plant tissue, as described previously (Zhou et al., 2014). After three washes in 540

RIPA buffer, samples were separated using 10% SDS-PAGE, transferred to polyvinylidene 541

diflouride membranes (Bio-Rad Laboratories), and detected with a mouse anti-GFP (1:2000; 542

632569; Takara Bio Inc.) or a mouse anti-tubulin (1:2000; 078K4842; Sigma-Aldrich) antibody. 543

Membranes were imaged using an Odyssey Clx Imaging system and fluorescence was quantified 544

using Image Studio software (LI-COR, inc). 545



20

Yeast Strains and Manipulations 546

All work with yeast was done using Saccharomyces cerevisiae strain NMY51:MATahis3D200 547

trp1-901 leu2-3,112 ade2 LYS2::(lexAop)4-HIS3 ura3::(lexAop)8-lacZ ade2::(lexAop)8-ADE2 548

GAL4 obtained from the DUAL membrane starter kit N (P01201-P01229). Yeast cells were 549

grown using standard microbial techniques and media (Lentze and Auerbach, 2008). Media 550

designations are as follows: YPAD is Yeast Extract plus Adenine medium, Peptone, and 551

Glucose; SD is Synthetic Defined dropout (SD-drop-out) medium. Minimal dropout media are 552

designated by the constituent that is omitted (e.g. “–-leu –trp –his –ade” medium lacks leucine, 553

tryptophan, histidine, and adenine). Recombinant plasmid DNA constructs were introduced into 554

NMY51 by LiOAc-mediated transformation as described (Gietz and Schiestl, 2007). 555

Statistical Analyses 556

The number of stomata analyzed for each line, in all figures, is ≥80, unless otherwise stated. 557

Error bars represent the standard deviation of means. Asterisks or symbols denote statistical 558

significance after Student’s t-test as indicated. 559

Accession Numbers 560

Sequence data from this article can be found in the GenBank/EMBL data libraries under 561

accession numbers NM_148591 (SINE1) and NM_111268 (SINE2).XXX. 562

563

Supplemental Data 564

The following materials are available in the online version of this article. 565

Supplemental Figure S1. Stomatal opening in sine mutants prior to exogenous application of 566

ABA. 567

Supplemental Figure S2. Stomatal closure in response to ABA for sine1-3 and sine2-2 mutants. 568

Supplemental Figure S3. Transpiration rates of individual leaves after induced stomatal 569

opening. 570



21

Supplemental Figure S4. Protein blot analysis of transgenic Arabidopsis plants expressing 571

GFP-SINE1 and GFP-SINE2. 572

Supplemental Figure S5. Interactions between SINE1 and SINE2 proteins in the membrane 573

yeast two-hybrid system. 574

Supplemental Figure S6. Stomatal density and stomatal index of fully developed rosette leaves. 575

Supplemental Figure S7. ROS production and cytoplasmic calcium monitoring in sine mutants. 576

Supplemental Figure S8. Root morphology of sine mutants. 577

Supplemental Table S1. Comparison of stomatal closure assays. 578

Supplemental Table S2. Percent stomatal closure for ABA and light-dark assays. 579

Supplemental Table S3. Percent stomatal closure for cytoskeleton drug treatment assays. 580

581

Acknowledgements 582

This work was funded by a National Science Foundation grant to I.M. (NSF-1613501). We are 583

grateful to Dr. Sarah Assmann (Penn State University) for critical reading of the first version of 584

this manuscript. We thank Andrew Kirkpatrick and all members of the Meier lab for fruitful 585

discussions and Dr. Norman Groves for proofreading, critiquing, and editing the final version of 586

the manuscript. We thank Dr. Xiao Zhou (Caribou Biosciences) for constructing the 35S-driven 587

SINE1 and SINE2 expressing Arabidopsis lines while working in the Meier lab and Dr. David 588

Mackey (OSU) for the fls2-1 mutant. 589

590



22

Figure legends: 591

Figure 1: Determining the role of SINE1 and SINE2 in the light regulation of stomatal 592

dynamics. (A) Stomatal imprints from intact whole Arabidopsis leaves were taken and stomatal 593

apertures were measured 2 h prior to the onset of lights (yellow bar) and every 2 h thereafter 594

until 2 h after lights off (black bar). Symbols denote statistical significance as determined by 595

Student’s t-test, with P<0.001. *: WT vs. all other lines; ǂ: sine1-1 vs. WT, SINE1:sine1-1, and 596

sine1-1 sine2-1; ¥: sine 2-1 vs. WT, SINE2:sine2-1, and sine1-1 sine2-1; (B) Whole leaves were 597

placed in specified buffer for 3 h under constant light at the end of a night cycle, epidermal peels 598

were mounted every 90 min, and stomatal apertures were measured. Top-left: opening buffer 599

(OB) base (see methods); Top-right: OB base plus 10 μM CaCl2; Bottom-left: OB base plus 20 600

mM KCl; Bottom-right: OB base plus 10 μM CaCl2 and 20 mM KCl. Symbols denote statistical 601

significance as determined by Student’s t-test, with P<0.001. *: specified lines vs WT; ǂ: 602

specified lines vs. SINE1:sine1-1; ¥: specified lines vs. SINE2:sine2-1; (C) Whole leaves were 603

placed in OB under constant light for 3 h and either kept under constant light or placed in dark 604

for an additional 3 h. Epidermal peels were taken and stomatal apertures were measured every 90 605

min after the initial 3 h stomatal opening phase. Symbols denote statistical significance as 606

determined by Student’s t-test, with P<0.001. *: dark WT vs light WT; ǂ: dark sine2-1 vs light 607

sine2-1. (A-C) All data are mean values ± SE from three independent experiments. 608

Figure 2: Abiotic vs. biotic stress induced stomatal changes in sine mutants. Stomatal 609

opening and closing assays were used here as described in methods. (A) Leaves incubated in 20 610

µM ABA during closure. All data were collected at the same time but are split here into two 611

panels for presentation purposes. WT and sine1-1 sine2-1 traces are therefore shown twice. (B) 612

Representative images of stomata for WT and sine1-1 lines before and after ABA exposure. (C) 613

Leaves were incubated in OB plus 20 µM ABA during stomatal opening. (D) Leaves incubated 614

in 5 µM flg22 during closure. All data are mean values ± SE from three independent 615

experiments. Symbols denote statistical significance as determined by Student’s t-test, with 616

P<0.001. *: specified lines vs. WT; ǂ: specified lines vs. SINE1:sine1-1; ¥: specified lines vs. 617

SINE2:sine2-1. 618



23

Figure 3: Transpiration rates after induced stomatal opening. Rosette leaves were taken 619

from 6-to 8-week-old short-day plants at similar developmental stages for each of the lines 620

depicted and kept abaxial side up. Fresh leaves were placed in specified buffer for 3 h under 621

constant light, transferred to a petri dish as specified below, and weighed every 30 min 622

thereafter. (A) In air; (B) in OB base; (C) in OB with representative images shown in (D) where 623

the top images are leaves at 0 min before OB incubation and bottom images are leaves after 180 624

min OB incubation. Mean values ± SE from at least three independent experiments are shown in 625

A-C. (B) shows no statistically significant differences. Symbols in (A) and (C) denote the 626

beginning of statistically significant differences as determined by Student’s t-test, with P<0.05. 627

*: sine1-1 vs. WT; ǂ: sine2-1 vs. WT; ¥: sine2-1 vs. SINE2:sine2-1; d: sine1-1 vs. SINE1:sine1-628

1. 629

Figure 4: Stomatal closure in response to H2O2 and CaCl2 for SINE1 and SINE2 mutants. 630

Stomatal opening and closing assays were used here as described in methods. (A-B) Leaves 631

incubated in 0.5 mM H2O2 during closure. Data obtained from one experiment and split into two 632

panels for clarity. (C-D) Leaves incubated in 2 mM CaCl2 during closure. Data obtained from 633

one experiment and split into two panels for clarity. (E) Leaves incubated in 0.5 mM H2O2 plus 2 634

mM CaCl2 during closure. All data are mean values ± SE from three independent experiments. 635

Symbols denote statistical significance as determined by Student’s t-test, with P<0.001. *: 636

specified lines vs. WT; ǂ: specified lines vs. GFP-SINE1:sine1-1; ¥: specified lines vs. GFP-637

SINE2:sine2-1. 638

Figure 5: SINE2 but not SINE1 overexpression leads to compromised stomatal dynamics. 639

(A) Confocal microscopy was used to take images of plants expressing GFP-tagged SINE1 or 640

SINE2, with representative images shown. Gain was set to first image of top row and used for 641

the remaining images. Scale bar represents 10 µm. (B) Data taken from two plants. ≥ 50 nuclei 642

were measured for each line. Nuclear fluorescence intensities were measured using ImageJ. 643

SINE2:sine2-1 had no measurable fluorescence signal at the nucleus and was therefore not 644

quantified. Symbols denote statistical significance as determined by Student’s t-test. *: P<0.005, 645

SINE2:WT vs. SINE1:sine1-1. (C) Stomatal apertures taken from stomatal imprint assay at the 646

start and end of light cycles. Symbols denote statistical significance as determined by Student’s 647

t-test. *: P<0.001, specified lines vs. WT; ǂ: P=0.004, specified lines vs. WT. (D) ABA induced 648



24

stomatal closure assay as described in methods. Symbols denote statistical significance as 649

determined by Student’s t-test, with *: P<0.001, specified lines vs. WT, SINE1:sine1-1, 650

SINE1:WT, and SINE2:sine2-1. Data shown in (C) and (D) are from three independent 651

experiments. Data are mean values ± SE. 652

Figure 6: Disrupting actin dynamics in sine1-1 and sine2-1 mutant lines alters stomatal 653

closure. Stomatal closure was monitored over a 3 h incubation time in the presence and absence 654

of ABA and actin disrupting drugs. (A) Buffers with and without 20 µM ABA and 10 µM of the 655

F-actin depolymerizing drug latrunculin B (LatB); Left: WT and sine1-1; Right: WT and sine2-1. 656

Symbols denote statistical significance as determined by Student’s t-test, with P<0.001. *: sine1-657

1, ABA+LatB vs. sine1-1, ABA only; ǂ: sine2-1, ABA+LatB vs. sine2-1, ABA only. (B) Buffers 658

with and without 20 µM ABA and 10 µM of the F-actin stabilizing drug jasplakinolide (JK); 659

Left: WT and sine1-1; Right: WT and sine2-1. Symbols denote statistical significance as 660

determined by Student’s t-test, with P<0.001. *: specified lines vs. sine1-1, ABA only; ǂ: sine1-1, 661

JK only vs. WT, JK only; ¥: sine1-1, ABA+JK vs. WT, ABA+JK. All data are mean values ± SE 662

from three independent experiments. 663

664

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836















Parsed CitationsAlbert R, Acharya BR, Jeon BW, Zañudo JGT, Zhu M, Osman K, Assmann SM (2017) A new discrete dynamic model of ABA-inducedstomatal closure predicts key feedback loops. PLoS Biol 15: e2003451

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Allen GJ, Kuchitsu K, Chu SP, Murata Y, Schroeder JI (1999) Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisicacid-induced cytoplasmic calcium rises in guard cells. Plant Cell 11: 1785-1798


An Y, Liu L, Chen L, Wang L (2016) ALA Inhibits ABA-induced Stomatal Closure via Reducing H2O2 and Ca(2+) Levels in Guard Cells.Front Plant Sci 7: 482


Chang W, Antoku S, Östlund C, Worman HJ, Gundersen GG (2015) Linker of nucleoskeleton and cytoskeleton (LINC) complex-mediated actin-dependent nuclear positioning orients centrosomes in migrating myoblasts. Nucleus 6: 77-88


Chang W, Worman HJ, Gundersen GG (2015) Accessorizing and anchoring the LINC complex for multifunctionality. J Cell Biol 208: 11-22


Coates JC (2003) Armadillo repeat proteins: beyond the animal kingdom. Trends Cell Biol 13: 463-471Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Daszkowska-Golec A, Szarejko I (2013) Open or close the gate - stomata action under the control of phytohormones in drought stressconditions. Front Plant Sci 4: 138


Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatalguard cells. J Exp Bot 55: 205-212


Dunning FM, Sun W, Jansen KL, Helft L, Bent AF (2007) Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeatdomain residues that contribute to flagellin perception. Plant Cell 19: 3297-3313


Eisenach C, Chen ZH, Grefen C, Blatt MR (2012) The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closureand K⁺ channel activity with vegetative growth. Plant J 69: 241-251


Eun SO, Lee Y (1997) Actin filaments of guard cells are reorganized in response to light and abscisic acid. Plant Physiol 115: 1491-1498Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005)AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis.Plant Cell 17: 3470-3488


Gietz RD, Schiestl RH (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31-34Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Gilroy S, Fricker MD, Read ND, Trewavas AJ (1991) Role of Calcium in Signal Transduction of Commelina Guard Cells. Plant Cell 3: 333-344


Grabov A, Blatt MR (1999) A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentrationincrease evoked by hyperpolarization in guard cells. Plant Physiol 119: 277-288

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon July 24, 2020 - Published by Downloaded from

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https://www.ncbi.nlm.nih.gov/pubmed?term=Albert R%2C Acharya BR%2C Jeon BW%2C Za�udo JGT%2C Zhu M%2C Osman K%2C Assmann SM %282017%29 A new discrete dynamic model of ABA%2Dinduced stomatal closure predicts key feedback loops%2E PLoS Biol 15%3A e&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Graumann K%2C Runions J%2C Evans DE %282010%29 Characterization of SUN%2Ddomain proteins at the higher plant nuclear envelope%2E Plant Journal&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Guzel Deger A%2C Scherzer S%2C Nuhkat M%2C Kedzierska J%2C Kollist H%2C Brosch� M%2C Unyayar S%2C Boudsocq M%2C Hedrich R%2C Roelfsema MR %282015%29 Guard cell SLAC1%2Dtype anion channels mediate flagellin%2Dinduced stomatal closure%2E New Phytol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Phosphatidic acid integrates calcium signaling and microtubule dynamics into regulating ABA-induced stomatal closure in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jiang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=PYR/PYL/RCAR abscisic acid receptors regulate K+ and Cl- channels through reactive oxygen species-mediated activation of Ca2+ channels at the plasma membrane of intact Arabidopsis guard cells&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

https://scholar.google.com/scholar?as_q=PYR/PYL/RCAR abscisic acid receptors regulate K+ and Cl- channels through reactive oxygen species-mediated activation of Ca2+ channels at the plasma membrane of intact Arabidopsis guard cells&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Xi W%2C Liu C%2C Hou X%2C Yu H %282010%29 MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis%2E Plant Cell&dopt=abstract

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

https://scholar.google.com/scholar?as_q=MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis&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

https://scholar.google.com/scholar?as_q=MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xi&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Xiao Y%2C Chen Y%2C Huang R%2C Chen J%2C Wang XC %282004%29 Depolymerization of actin cytoskeleton is involved in stomatal closure%2Dinduced by extracellular calmodulin in Arabidopsis%2E Sci China C Life Sci&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Depolymerization of actin cytoskeleton is involved in stomatal closure-induced by extracellular calmodulin in Arabidopsis&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

https://scholar.google.com/scholar?as_q=Depolymerization of actin cytoskeleton is involved in stomatal closure-induced by extracellular calmodulin in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xiao&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yin Y%2C Adachi Y%2C Ye W%2C Hayashi M%2C Nakamura Y%2C Kinoshita T%2C Mori IC%2C Murata Y %282013%29 Difference in abscisic acid perception mechanisms between closure induction and opening inhibition of stomata%2E Plant Physiol&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Difference in abscisic acid perception mechanisms between closure induction and opening inhibition of stomata&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

https://scholar.google.com/scholar?as_q=Difference in abscisic acid perception mechanisms between closure induction and opening inhibition of stomata&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yin&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang JF%2C Yuan LJ%2C Shao Y%2C Du W%2C Yan DW%2C Lu YT %282008%29 The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis%2E Plant Cell Environ&dopt=abstract

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

https://scholar.google.com/scholar?as_q=The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis&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

https://scholar.google.com/scholar?as_q=The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang W%2C He SY%2C Assmann SM %282008%29 The plant innate immunity response in stomatal guard cells invokes G%2Dprotein%2Ddependent ion channel regulation%2E Plant J&dopt=abstract

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

https://scholar.google.com/scholar?as_q=The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation&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

https://scholar.google.com/scholar?as_q=The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhao S%2C Jiang Y%2C Zhao Y%2C Huang S%2C Yuan M%2C Guo Y %282016%29 CASEIN KINASE1%2DLIKE PROTEIN2 Regulates Actin Filament Stability and Stomatal Closure via Phosphorylation of Actin Depolymerizing Factor%2E Plant Cell&dopt=abstract

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

https://scholar.google.com/scholar?as_q=CASEIN KINASE1-LIKE PROTEIN2 Regulates Actin Filament Stability and Stomatal Closure via Phosphorylation of Actin Depolymerizing Factor&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

https://scholar.google.com/scholar?as_q=CASEIN KINASE1-LIKE PROTEIN2 Regulates Actin Filament Stability and Stomatal Closure via Phosphorylation of Actin Depolymerizing Factor&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhao Y%2C Zhao S%2C Mao T%2C Qu X%2C Cao W%2C Zhang L%2C Zhang W%2C He L%2C Li S%2C Ren S%2C Zhao J%2C Zhu G%2C Huang S%2C Ye K%2C Yuan M%2C Guo Y %282011%29 The plant%2Dspecific actin binding protein SCAB1 stabilizes actin filaments and regulates stomatal movement in Arabidopsis%2E Plant Cell&dopt=abstract

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

https://scholar.google.com/scholar?as_q=The plant-specific actin binding protein SCAB1 stabilizes actin filaments and regulates stomatal movement in Arabidopsis&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

https://scholar.google.com/scholar?as_q=The plant-specific actin binding protein SCAB1 stabilizes actin filaments and regulates stomatal movement in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou X%2C Graumann K%2C Evans DE%2C Meier I %282012%29 Novel plant SUN%2DKASH bridges are involved in RanGAP anchoring and nuclear shape determination%2E J Cell Biol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination&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

https://scholar.google.com/scholar?as_q=Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


diverse functions in plants. J Cell Biol 205: 677-692Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhou X, Groves NR, Meier I (2015) SUN anchors pollen WIP-WIT complexes at the vegetative nuclear envelope and is necessary forpollen tube targeting and fertility. J Exp Bot 66: 7299-7307


Zhou X, Meier I (2013) How plants LINC the SUN to KASH. Nucleus 4: 206-215Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

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



https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou X%2C Graumann K%2C Wirthmueller L%2C Jones JD%2C Meier I %282014%29 Identification of unique SUN%2Dinteracting nuclear envelope proteins with diverse functions in plants%2E J Cell Biol&dopt=abstract


https://scholar.google.com/scholar?as_q=Identification of unique SUN-interacting nuclear envelope proteins with diverse functions in plants&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

https://scholar.google.com/scholar?as_q=Identification of unique SUN-interacting nuclear envelope proteins with diverse functions in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou X%2C Groves NR%2C Meier I %282015%29 SUN anchors pollen WIP%2DWIT complexes at the vegetative nuclear envelope and is necessary for pollen tube targeting and fertility%2E J Exp Bot&dopt=abstract


https://scholar.google.com/scholar?as_q=SUN anchors pollen WIP-WIT complexes at the vegetative nuclear envelope and is necessary for pollen tube targeting and fertility&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

https://scholar.google.com/scholar?as_q=SUN anchors pollen WIP-WIT complexes at the vegetative nuclear envelope and is necessary for pollen tube targeting and fertility&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou X%2C Meier I %282013%29 How plants LINC the SUN to KASH%2E Nucleus&dopt=abstract


https://scholar.google.com/scholar?as_q=How plants LINC the SUN to KASH&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

https://scholar.google.com/scholar?as_q=How plants LINC the SUN to KASH&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://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&dopt=abstract

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

https://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

https://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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Short title: SINE proteins function in stomatal dynamics · 127 conditions. On average, neither sine1-1 nor sine2-1 stomata were fully open or fully closed for 128 the duration of