2 Update on Mitochondrial Reactive Oxygen Species 3 · 2 Update on Mitochondrial Reactive Oxygen Species 3 4 The roles of mitochondrial reactive oxygen species in cellular signalling

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1 Update on Mitochondrial Reactive Oxygen Species 2 3

The roles of mitochondrial reactive oxygen species in cellular signalling and 4

stress response in plants 5

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Shaobai Huang1, Olivier Van Aken1, Markus Schwarzländer2, 7

Katharina Belt1, A. Harvey Millar1* 8

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1. ARC Centre of Excellence in Plant Energy Biology, The University of Western 10

Australia, 35 Stirling Highway, Crawley WA 6009, Australia. 11

2. Plant Energy Biology Lab, Institute of Crop Science and Resource Conservation 12

(INRES), University of Bonn, Friedrich-Ebert-Allee 144, 53113 Bonn, Germany 13

14 *Corresponding author: 15 A. Harvey Millar, [email protected]; Ph +61 8 64887245 16 17

One-sentence Summary 18

Generation of reactive oxygen species by plant mitochondria contributes to cellular 19 signalling and stress response. 20

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Author contributions: A.H.M and S.H. conceived the review. S.H., O.V.A, M.S and 22 K.B contributed draft sections in their areas of expertise. All authors were involved in 23 assembling the review and discussed and revised the text based on their expertise. 24

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Funding Agencies 26

This work was supported by the facilities of the Australian Research Council Centre 27 of Excellence Program (CE140100008). MS thanks the Deutsche 28 Forschungsgemeinschaft (DFG) for support through the Emmy-Noether programme 29 (SCHW1719/ 1-1), the Research Training Group GRK2064 and a grant 30 (SCHW1719/5-1) as part of the package PAK918. SH and AHM were funded as 31 ARC Australian Future Fellows (FT130101338; FT110100242 respectively). OVA is 32 supported in part by ARC Discovery Projects (DP130102918 and DP160103573). 33

Plant Physiology Preview. Published on March 28, 2016, as DOI:10.1104/pp.16.00166

Copyright 2016 by the American Society of Plant Biologists

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KB holds a SIRF (Scholarship for International Research Fees) and UIS (University 34 International Stipend) from the University of Western Australia. 35

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Abstract 39 Mitochondria produce ATP via respiratory oxidation of organic acids and transfer of 40 electrons to O2 via the mitochondrial electron transport chain (mtETC). This process 41 produces reactive oxygen species (ROS) at various rates which can impact on 42 respiratory and cellular function, affecting a variety of signalling processes in the cell. 43 Roles in redox signalling, retrograde signalling, plant hormone action, programmed 44 cell death, and defence against pathogens have been attributed to ROS generated in 45 plant mitochondria (mtROS). The shortcomings of the black-box-idea of mtROS are 46 discussed in the context of mechanistic considerations and the measurement of 47 mtROS. The overall aim of this update is to better define our current understanding of 48 mtROS and appraise their potential influence on cellular function in plants. 49 Furthermore, directions for future research are provided, along with suggestions to 50 increase reliability of mtROS measurements. 51 52 Generation of mitochondrial ROS 53 Molecules typically referred to as ROS in plant cells include ozone, singlet oxygen, 54 superoxide, H2O2, and the hydroxyl radical. There is no reliable information on any 55 significant generation of ozone and singlet oxygen by plant mitochondria, and the 56 short half-life of the hydroxyl radical makes it incompatible with specific roles in signal 57 transduction through selective modification of target molecules. This leaves 58 superoxide and H2O2 as good candidates for mtROS of regulatory significance. 59 Superoxide is formed through single electron reduction of O2 and the respiratory 60 Complexes I, II and III have all been identified as major production sites, but display 61 fundamentally different rates and topologies of superoxide release (Murphy, 2009). 62 The relative physiological contributions of each also remain notoriously hard to 63 dissect. Plant-focussed studies have provided some mechanistic insight (Rich and 64 Bonner Jr, 1978; Møller, 2001; Gleason et al., 2011; Jardim-Messeder et al., 2015), 65 but the bulk of the evidence is still derived from more detailed mammalian studies 66 (Murphy, 2009). While superoxide production occurs during normal operation of the 67 respiratory chain, its rate is strongly increased when respiratory rate is slowed down, 68 e.g. by restricted ADP availability or respiratory chain inhibition, leading to a highly 69 reduced state of mtETC components (Møller, 2001). 70 71 Superoxide production by the mtETC can be minimised by a variety of pathways in 72 plant mitochondria that bypass the classical mtETC and oxidative phosphorylation. 73 Uncoupling proteins (UCPs) promote proton leak across the membrane (Sweetlove 74 et al., 2006) while NDs and AOXs bypass proton pumping by electron flow via 75



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Complex I, and Complex III and IV, respectively. The role of AOX in minimising ROS 76 production has been extensively reviewed (Rhoads et al., 2006; Vanlerberghe, 77 2013). Recently, overexpression of the Arabidopsis uncoupler protein UCP1 in 78 tobacco was found to reduce the rate of ROS generation, induce the antioxidant 79 defense system and enhance resistance to multiple abiotic stresses (Barreto et al., 80 2014). Superoxide spontaneously disproportionates to H2O2 and O2, but this can be 81 strongly accelerated by superoxide dismutase (SOD) (Møller, 2001; Morgan et al., 82 2008). Alternatively, superoxide readily reacts with other radicals such as NO or 83 redox-active metal centres of other proteins (Tan et al., 2010). These reactions 84 outcompete interactions with abundant biomolecules such as the amino acid residues 85 of proteins, nucleic acids, lipids and sugars. Suppression of the mitochondrial matrix 86 manganese SOD in Arabidopsis disturbs thiol redox homeostasis of the matrix, 87 retards root growth (Morgan et al., 2008) and leads to disruption of female 88 gametogenesis (Martin et al., 2013). The H2O2 released by the matrix SOD can either 89 be removed on site or exit the matrix. In both cases efficient detoxification systems 90 are in place and selective oxidation of regulatory targets may relay information on 91 mitochondrial processes. 92 93 ROS signalling within mitochondria by thiol switching? 94 Specific protein thiols may be oxidized by H2O2. Several studies have found redox-95 active thiols on matrix proteins, some of which have been shown to adjust protein 96 function in vitro, raising the possibility of intra-mitochondrial ROS-dependent thiol 97 redox signalling to adjust functions at the protein level. Examples that have been 98 specifically characterized include AOX (Yoshida et al., 2013) and several TCA-cycle 99 enzymes (Schmidtmann et al., 2014; Yoshida and Hisabori, 2014; Daloso et al., 100 2015), with the TRX system as the likely endogenous reductant. Gel-based redox 101 proteomics and TRX-trapping approaches have identified even more mitochondrial 102 proteins that can – in principle - undergo thiol switching (Winger et al., 2007; Yoshida 103 et al., 2013). For all of these proteins it remains unresolved if the respective thiol 104 switch can be oxidized by mtROS (directly or indirectly) and maintained in its oxidized 105 state, considering the presence of a highly efficient re-reduction system under 106 physiological conditions. A switch would be a prerequisite for bona fide redox-107 regulation, as opposed to TRX-mediated ‘maintenance’ of a thiol in its reduced state. 108 A particularly intriguing example of intra-mitochondrial thiol redox regulation has been 109 studied in mammals where Complex I can be deactivated by reversible oxidation of a 110 Cys-39 of ND3 (Chouchani et al., 2013) to avoid excessive superoxide release from 111 reverse electron flow at re-oxygenation after anoxia. The Cys motif at ND3 is well-112 conserved in plants (Cys-45 in Arabidopsis) (Braun et al., 2014) but evidence for 113 reverse electron flow is currently lacking in plants. However, given the conservation it 114 appears worthwhile to investigate its potential plant function, such as during the 115 recovery from water-logging. 116 117 Measuring mtROS in vitro and in vivo 118



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The generation of mtROS is routinely studied using colorimetric and fluorescent 119 detection systems. Probes such as 3,3’-diaminobezidine (DAB), nitroblue tetrazolium 120 (NBT), AmplexRed (for isolated mitochondria), 2’,7’-dichlorofluorescein (DCF) 121 derivatives and hydroethidine (HE) have been reported to detect or even quantify 122 H2O2, superoxide or ‘mtROS’ in plant studies (Gleason et al., 2011; Li and Xing, 123 2011; Martin et al., 2013). However there are legitimate concerns about their 124 specificity, subcellular accumulation and their interference with endogenous redox 125 biology (Bonini et al., 2006; Zielonka and Kalyanaraman, 2010; Miwa et al., 2016), 126 prompting the search for straightforward and applicable alternatives. Probes that can 127 be specifically placed in mitochondria, either through electrical potential-driven 128 accumulation (e.g., MitoSOX Red) (Miller et al., 2009; Li and Xing, 2011; Martin et al., 129 2013; Liu et al., 2014) or through genetic targeting for fluorescent protein sensors 130 (Schwarzländer et al., 2016) have addressed the localisation issue. However, their 131 chemical specificity in mitochondria also remains a concern. For example, cpYFP 132 that was reported as responsive to superoxide and has been used as such also in 133 plant mitochondria (He et al., 2012) has been conclusively shown not to react to 134 superoxide, but to pH changes (Schwarzländer et al., 2014), while the H2O2-135 responsive HyPer family of fluorescent protein probes (Costa et al., 2010) also suffer 136 from pH artefacts, making measurements in the matrix, where pH can change rapidly 137 (Schwarzländer et al., 2012), problematic. Dynamic measurements using such 138 probes also rely on efficient probe regeneration after oxidation via the endogenous 139 glutathione/glutaredoxin system. Yet, the only known matrix GRX (GRXS15) shows 140 very low thiol exchange activity (Moseler et al., 2015; Stroeher et al., 2016). Rigorous 141 application and further optimization of HyPer probes as well as peroxidase-coupled, 142 pH-insensitive roGFP sensors, like roGFP2-Orp1 (Gutscher et al., 2009), appear to 143 offer the best potential to allow specific measurements of a defined mtROS (H2O2) 144 and allow physiological interpretation. This may be complemented by mass-145 spectrometry based approaches that have been developed in mammalian 146 mitochondria (Cochemé et al., 2011), but have not yet been used in plants. 147 148 Given the persisting methodological constraints, it is important to note that most 149 historical reports of ‘mtROS production’ in planta are only one interpretation of the 150 chosen monitoring technique (i.e., chemical reaction product, optical probe, marker 151 metabolite or marker transcript), and are often based on assumptions that may or 152 may not be justified in a particular case as discussed above. Future experiments 153 should involve a transparent appraisal of the chosen technique or cellular mtROS 154 indicator, which will allow accumulating evidence from orthogonal approaches across 155 studies to paint a clearer picture. 156 157 158 Considerations for transduction of mtROS signals out to the cell 159 Movement of mtROS signals out of mitochondria requires a direct and sensitive 160 target and a means of transducing the signals from the various intra-mitochondrial 161 locations to the cytosol. If there is a direct downstream target of a mitochondrial 162



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superoxide signal, proteins with transition metal cofactors are likely to be the first 163 candidates. An intriguing mechanism has been proposed in yeast and mammals by 164 which the activity of cytosolic SOD1 controls mitochondrial respiration (Reddi and 165 Culotta, 2013), but plants have not yet been investigated for comparable signalling. 166 Efficient dismutation of superoxide inside mitochondria, however, makes H2O2 a 167 more likely signal, aided by its much longer estimated lifetime and the ability for 168 channel-mediated membrane passage through aquaporins (Bienert and Chaumont, 169 2014). At least one aquaporin (TIP5;1) can localize to the mitochondria in 170 Arabidopsis (Soto et al., 2010). However, the reactivity of H2O2 is also remarkably 171 limited by kinetic competition and most thiols are not particularly reactive for H2O2 172 within the cellular environment in the absence of catalysis. Exceptions, however, can 173 be found in thiols of a small group of proteins that have been found enriched in 174 mitochondria (Riemer et al., 2015). Particularly interesting are the thiol peroxidases, 175 which have been recognized as amongst to most H2O2-reactive thiols in cells 176 (Perkins et al., 2015) and are key players in H2O2 detoxification in plants (Dietz, 177 2011). With PrxII F and a GPX-like protein, two thiol peroxidases have so far been 178 found in plant mitochondria (Finkemeier et al., 2005; Navrot et al., 2006). Low Kd and 179 high reactivity of the catalytic peroxiredoxin thiols can generate specific H2O2 drains 180 that outcompete other thiols and ensure that a large part of H2O2 turnover flux will be 181 focussed to one specific thiol (Veal et al., 2007). This would provide kinetic control of 182 H2O2 dynamics in vivo keeping ambient H2O2 levels low and protecting other 183 biomolecules from oxidation. To serve as a signal this information must be 184 conserved, perhaps by dividing regeneration into a rapid-turnover high-flux 185 antioxidant pathway and a slow-turnover low-flux signalling pathway, with their 186 relative contributions set by distinct biochemical properties. Once translated, the 187 H2O2 signal could then regulate downstream protein targets by a thiol switch or be 188 further transduced by thiol-redox signalling (Riemer et al., 2015). This provides a 189 means to quantify H2O2 flux by ‘counting’ molecules detoxified at a specific location. 190 Maintaining information on the location of H2O2 sensing appears critical to 191 discriminate between stimuli from distinct sources and to mount specific responses. 192 Oxidation of mitochondrial proteins followed by proteolysis and export of the peptides 193 has been proposed as a scenario of this general concept (Møller and Sweetlove, 194 2010). Indeed oxidative modification has been observed for plant mitochondrial 195 proteins (Kristensen et al., 2004; Tan et al., 2010), but further work will be required to 196 clarify to what extent this occurs under physiological conditions in vivo. 197 198 Increasing experimental evidence supports the concept of co-localisation of ROS-199 signal and ROS-sensing. Recently mtETC-derived H2O2 were shown to be perceived 200 in the IMS triggering a phosphorylation cascade in animals (Patterson et al., 2015). 201 As the interface between the mitochondrion and the rest of the cell, the IMS hosts its 202 own redox machinery, which may make it well-suited as the integration site to 203 prepare mtETC-derived ROS signals for transduction across the cell before they get 204 quenched by the strong antioxidant defences of the cytosol. Placing the ROS-205 sensing system close to the mitochondrial surface, where H2O2 is thought to pass the 206



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OMM via porins offers similar properties. Contact sites between ER and mitochondria 207 may act as such hotspots (Jaipargas et al., 2015; Müller and Reski, 2015). Although 208 the exact mechanism remains to be determined, thiol-switch-based sensing of 209 mitochondrial-derived H2O2 at ER contact sites makes an attractive hypothesis. The 210 reverse, i.e. H2O2 produced by the ER to be sensed within the mitochondrial matrix 211 inducing glutathionylation of a glycine decarboxylase subunit, has been proposed 212 recently (Hoffmann et al., 2013). A recent study suggests that the twin-cysteine 213 proteins At12cys1/2 can relocate from the mitochondria to cytosol and chloroplast 214 upon Complex I dysfunction, providing a potential mechanism to signal mitochondrial 215 dysfunction to the rest of the cell in plants (Wang et al., 2016). 216 217 218 mtROS and retrograde signalling 219 Mitochondria can signal information about their functional status to the nucleus, 220 leading to targeted transcriptional responses, a process often described as 221 mitochondrial retrograde regulation (MRR) (Rhoads and Subbaiah, 2007; Ng et al., 222 2014). Many factors involved in the transcriptional regulation of MRR have been 223 identified and belong to a range of functional classes, including transcription factors 224 (NAC, WRKY, ABI4) and cyclin-dependent kinases (CDKE;1)(Ng et al., 2014). Also 225 an antagonistic relationship between auxin and retrograde signalling has been 226 shown in a variety of mutant backgrounds (including PIN1, BIG and AS1) (Ivanova et 227 al., 2014). Surprisingly, MRR-mediators ANAC013 and ANAC017 are bound to the 228 endoplasmic reticulum (De Clercq et al., 2013; Ng et al., 2013). Upon stress, they 229 are thought to be released and relocate to the nucleus to exert transcriptional 230 regulation. This identified the ER as a key signalling intermediate in MRR, and based 231 on inhibitor studies the proteolytic release of NAC TFs may be mediated by 232 rhomboid-class proteases (Ng et al., 2013). 233

The identity of the signal(s) that relays information from a dysfunctional 234 mitochondrion via the ER to the downstream transcription factor cascades, currently 235 remains unknown. Evidence so far suggests that TCA cycle intermediates like citrate 236 have relatively mild transcriptional effects, and TCA-intermediate signalling does not 237 appear to occur via the NAC pathway, as the affected genes are very different 238 (Finkemeier et al., 2013). However, several individual findings point towards a role 239 for mtROS and taken together they make a strong case. One of the most commonly-240 used ways of triggering MRR in plants has been treatment with complex III inhibitor 241 antimycin A (AA). AA treatment is well established to induce retrograde marker 242 genes such as AOX1a in Arabidopsis (Dojcinovic et al., 2005; Ng et al., 2013). AA 243 application to plant cells induced increased ROS production as detected by DCF 244 accumulation in the mitochondria (Maxwell et al., 1999), suggesting that the ROS 245 produced by AA could act as signalling intermediates. Further in line with a signalling 246 role for mtROS, AA-induced retrograde signalling was suppressed when ROS 247 production was reduced by overexpression of AOX in tobacco (Maxwell et al., 1999). 248

Also other studies indirectly suggest a correlation between mitochondrial defects, 249 (mt)ROS formation and retrograde signalling. For example, Complex I subunit 250 ndufs4 mutants have higher basal superoxide production rate as measured by NBT 251



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staining, as well as constitutive retrograde marker gene expression (Meyer et al., 252 2009). Other studies have looked at nuclear transcription in backgrounds with 253 mtROS-related enzymes, such as manganese SOD msd1 knock-down plants, and 254 AA treatment in peroxiredoxin II F prxII F mutants compared to WT ( Schwarzländer 255 et al., 2012). However, both studies showed relatively weak transcriptional changes 256 in common MRR marker genes, so it is difficult to draw clear conclusions for the role 257 of mtROS in retrograde signalling from these experiments. 258

More evidence for a role of mtROS in retrograde signalling comes from the 259 observation that MRR responses show remarkable overlaps with transcriptional 260 responses to different ROS triggers and abiotic stress, e.g H2O2 and salt stress. This 261 is the case both for chemically-induced MRR, as well as MRR caused by genetic 262 defects in mitochondrial components (Van Aken et al., 2007; Meyer et al., 2009; Van 263 Aken and Whelan, 2012). Furthermore, many of the core ANAC017-dependent 264 transcripts affected by AA also showed altered responses to H2O2 application (Ng et 265 al., 2013). Remarkably, 87% of transcript changes caused by H2O2 were affected in 266 anac017 mutants. This indicates that ANAC017 is a key regulator of H2O2 responses, 267 and that at least one avenue for ROS production may be via mitochondria. Future 268 work will be required to understand how mtROS signals would trigger such MRR 269 response in a mechanistic way. 270 271 mtROS and plant hormone signalling 272 Plant hormones play a key role in regulating growth and development and in 273 response to stresses. Hormone - ROS interactions have recently been reviewed (del 274 Río, 2015), as well as links between MRR regulation and hormone signalling 275 (Berkowitz et al., 2016). Both connections have recently been brought together by 276 accumulating evidence indicating that mitochondria play a role in regulation of plant 277 hormone signalling, such as ABA and auxin, and that mtROS may be key 278 intermediates. 279 280 Evidence for an interplay between ABA and mitochondria via mtROS has been found 281 in lines with different sensitivity to ABA (Laluk et al., 2011; He et al., 2012; Murayama 282 et al., 2012; Sechet et al., 2015). Collectively these reports show that the underlying 283 causes of increased ABA sensitivity in a range of mutants are mitochondrial defects. 284 In some of these mutants increases in ROS were reported, while others report 285 decrease, using a variety of different detection methods. Given that mitochondria are 286 crucial during early germination and seedling establishment (both are repressed by 287 ABA) (Howell et al., 2006; Wang et al., 2014), it appears conceivable that 288 mitochondrial mutants are particularly susceptible to unfavourable germination 289 conditions. While more evidence is required to test if mtROS have a direct role in 290 ABA signalling, transcription of a range of genes encoding mitochondrial proteins is 291 clearly responsive to ABA (Van Aken et al., 2009; Wang et al., 2014). 292 293 Regulation of auxin homeostasis has been linked to increased ROS levels (Tognetti 294 et al., 2012) and mitochondria have been suggested to be involved. By screening for 295



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more axillary shoot (mas) mutants, mitochondrial AAA-protease AtFtSH4 was 296 identified. Loss of FtSH4 function resulted in a reduction in protein stability in the 297 mitochondria and increased H2O2 levels, which may be used for peroxidase-mediated 298 oxidation of IAA and cause excessive axillary branches and a dwarf phenotype 299 (Zhang et al., 2014). Also overexpression of mitochondrial AtPHB3 or MRR/ROS-300 signalling target gene UGT74E2 (an auxin glycosyltransferase) results in profuse 301 shoot branching (Van Aken et al., 2007; Tognetti et al., 2010). It has previously been 302 shown that ftsh4 mutants show induction of a number of MRR/ROS marker genes, 303 providing further links between mtROS signalling and auxin homeostasis (Gibala et 304 al., 2009). 305 306 Treatment with AA resulted in decreased IAA levels and changes in other genes 307 related to auxin conjugation, transportation and receptors (Ivanova et al., 2014). In 308 reverse, treatments or mutations that block polar auxin transport (e.g. pin1) result in a 309 hyperactivated MRR response to AA (Ivanova et al., 2014; Kerchev et al., 2014). This 310 antagonistic relationship between auxin and MRR could provide the plant with a 311 switching mechanism between growth under optimal conditions (no MRR signals, 312 auxin-stimulated growth), and growth-arrest during stress conditions (MRR signalling 313 negatively affects auxin-induced growth). Furthermore, it may allow the plant to 314 reverse MRR-induced growth arrests when the mitochondrial dysfunction has been 315 resolved. 316 317 318 mtROS in programmed cell death and pathogen response 319 MtROS production in plants has been implicated in the execution of programmed cell 320 death (PCD) (Van Aken and Van Breusegem, 2015). Great efforts have been made 321 to validate relatively well-described yeast or animal PCD pathways in plants; yet with 322 limited success. For instance, cytochrome c release, which is also observed in plants 323 during HR-induced PCD, may merely reflect a final phase of mitochondrial 324 dysfunction, rather than an initial step of the process (Yao et al., 2004). MtROS 325 production is often increased during stress and PCD, likely due to mtETC inhibition. 326 Several studies support this by showing that mtETC enzymes, such as AOX, protect 327 against PCD (Li and Xing, 2011; Liu et al., 2014; Wu et al., 2015). A recent study 328 showed that mitochondrial Complex I is responsible for the ROS production that 329 leads to PCD in the Arabidopsis mosaic death 1 (mod1) mutant, even though the 330 MOD1 protein is active in chloroplasts (Wu et al., 2015). A critical role for mtROS, but 331 not apoplastic or chloroplast ROS, has also been suggested in harpin-induced PCD 332 (Garmier et al., 2007). 333 334 Mitochondria have also been proposed to be linked with PCD via increased ROS 335 production during pathogen defence, such as during the hypersensitive response 336 (HR) (Lam et al., 2001; Mur et al., 2008; Van Aken and Van Breusegem, 2015). In 337 agreement, a wide variety of mutants in mitochondrial functions have been reported 338 to have altered PCD or pathogen defence phenotypes. Upon infection with the 339



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bacterial pathogen Pseudomonas syringae and PPIX treatment, Arabidopsis protein 340 ACD2 (Accelerated Cell Death 2) changed its location from chloroplastic to both 341 chloroplastic and mitochondrial (Yao and Greenberg, 2006). More recent work 342 showed that the ACD2-substrate red chlorophyll catabolite (RCC), a toxic chlorophyll-343 breakdown product that can trigger ROS production, can shift to mitochondria to 344 cause ROS-induced PCD (Pattanayak et al., 2012). This suggests that mitochondrial 345 ROS formation may be the key cause of PCD induction in acd2 mutants, further 346 supported by the observation that ectopic targeting of antioxidant enzymes like 347 ascorbate peroxidase and catalase to the mitochondria can suppress PCD (Yao and 348 Greenberg, 2006). 349 350 Perturbations in the mtETC that are linked to ROS metabolism can result in altered 351 pathogen susceptibility. A well-known example came from analysis of N. sylvestris 352 CMSII line with complex I (NAD7) deficiency (Garmier et al., 2002; Dutilleul et al., 353 2003b). There are dramatic differences in antioxidant and defense gene expression 354 between wild-type and CMSII leaves inoculated with a bacterial elicitor (Garmier et 355 al., 2002). CMSII(N) plants have higher resistance to TMV than wild-type plants, 356 mainly due to the inhibition of the virus by the high level of leaf antioxidant enzymes 357 (Dutilleul et al., 2003b). During Erwinia amylovora hairpin-induced HR, this CMSII 358 line showed impaired AOX engagement, but an increase in mitochondrial SOD 359 activity and antioxidant capacity (Vidal et al., 2007). 360 361 Further evidence for a role of mtROS in PCD comes from a recent finding that 362 spontaneous PCD lesion formation in the mod1 mutant with deficiency in fatty acid 363 biosynthesis can be suppressed by genetic impairment of Complex I (Wu et al., 364 2015). Also treatment with Complex I inhibitor rotenone could partially suppress PCD. 365 This work indicates that deficiencies in Complex I can result in decreased ROS 366 production, and compromise HR and resistance against bacteria (Wu et al., 2015). 367 To address whether mtROS or ATP status regulate PCD, the authors showed that 368 overexpression of cytosolic Cu/Zn SOD could suppress PCD, suggesting that ROS is 369 indeed causative (at least potentially mitochondrial ROS that reaches the cytosol). 370 This study also indicated that the ROS generated by the plasma membrane NADPH 371 oxidase is not directly involved in mod1 PCD, emphasizing that formation of ROS 372 through the mtETC likely initiates the PCD process (Wu et al., 2015). 373 374 Complex II subunit SDH1-1 was found to act as intermediate in a signal transduction 375 pathway that induces promoter activity of salicylic acid-responsive plant defense 376 genes (Gleason et al., 2011). Moreover, the effect of the mutation could be overcome 377 by triggering promoter activity with exogenous H2O2, suggesting that the effect of 378 SDH1-1 lies upstream of ROS presence. Indeed, this mutant showed less mtROS 379 production, and was more susceptible to several pathogens (Gleason et al., 2011), 380 indicating the importance of mitochondrial function in pathogen defenses via ROS 381 production. The slo2 mutant, for which reductions in Complexes I, III, and IV have 382



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been reported along with increased ROS levels, is also more susceptible to the 383 necrotrophic pathogen Botrytis cinerea (Zhu et al., 2014). 384 385 AOX has also been reported to be involved in plant defense against bacterial, viral 386 and fungal pathogens via regulation of ROS metabolism (Cheng et al., 2011; Lee et 387 al., 2011; Cvetkovska and Vanlerberghe, 2012; Zhang et al., 2012; Cvetkovska and 388 Vanlerberghe, 2013). Differential expression of AOX and MnSOD transcripts at 389 pathogen exposure and HR indicates a complex response pattern (Cvetkovska and 390 Vanlerberghe, 2012, 2013). Silencing of AOX resulted in an increase of detectable 391 matrix superoxide (Cvetkovska and Vanlerberghe, 2012). Furthermore, in AOX RNAi 392 lines the threshold for cell death at inhibition of the cytochrome pathway by AA was 393 lowered (Cvetkovska and Vanlerberghe, 2012, 2013), while AOX overexpression 394 prevented HR and plant cell death (Vanlerberghe et al., 2002). 395 396 Non-mtETC proteins have reported roles in plant pathogen defense. A gene 397 encoding mitochondrial inner membrane protein PAM16, connected to the TIM23 398 translocase complex, was identified as negative regulator of R-protein (Huang et al., 399 2013). The atpam16 mutant has increased levels of PR1 and PR2 transcript, 400 increased ROS production as measured by a luminol-based assay and DAB staining, 401 smaller rosette size and enhanced resistance to virulent pathogen attack (Huang et 402 al., 2013). AtPAM16 may be involved in the import of a negative regulator of plant 403 immunity to the mitochondrial matrix, which could function as a modulator of ROS 404 generation (Huang et al., 2013). Plants overexpressing the mitochondrial outer 405 membrane AAA ATPase AtOM66 also have increased basal ROS production (NBT 406 staining) and expression of SA marker gene PR1 (Zhang et al., 2014). AtOM66 over-407 expression plants show increased SA content, accelerated cell death rates and have 408 altered pathogen resistance (Zhang et al., 2014). The Arabidopsis defence protein 409 PEN2 has recently been found to hyper-accumulate on the outer membrane of 410 mitochondria that cluster around infection sites of leaf epidermal cells (Fuchs et al., 411 2015). Redox sensing revealed an oxidative shift in the matrix glutathione pool of 412 mitochondria at the infection site in relation to other parts of the same cell or 413 neighbouring cells. This observation is suggestive of specialized functions of 414 mitochondrial subpopulations within a cell, which may include strictly localized ROS-415 linked immune responses. 416 417 In tomato, mitochondrial alpha-ketoglutarate dehydrogenase (Slα-kGDH) E2 binds 418 salicylic acid (SA), and Slα-kGDH E2 silencing increased resistance to tobacco 419 mosaic virus in an AOX-dependent way (Liao et al., 2015). Finally, a role of 420 mitochondrial proline metabolism in mtROS production and PCD has been emerging. 421 Proline levels increase during HR and the transcripts of proline dehydrogenase 422 (ProDH1 and ProDH2) are induced by SA in Arabidopsis (Cecchini et al., 2011). 423 Furthermore, silencing of ProDH1 and ProDH2 in Arabidopsis reduces ROS levels 424 after pathogen infection, but makes plants more susceptible to avirulent pathogens 425 (Cecchini et al., 2011; Senthil-Kumar and Mysore, 2012). Similarly, silencing of 426



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mitochondrial ornithine delta-aminotransferase (dOAT) and proline dehydrogenases 427 in N. benthamiana delayed occurrence of HR and favoured non-host pathogen 428 growth (Senthil-Kumar and Mysore, 2012). How ROS is produced by proline 429 metabolism is not entirely clear, with some suggestion that pyrroline-5-carboxylate 430 (P5C) to proline cycling is indirectly responsible, or that P5C itself can cause ROS 431 and PCD (Qamar et al., 2015). For instance, overexpression of P5C dehydrogenase 432 increases the resistance of plants to P5C-induced HR-like PCD and ROS production 433 (Miller et al., 2009). 434 435 436 437 Conclusion and Perspectives 438 Plant mtROS are primarily produced, and their rate of production is controlled, by the 439 kinetics of the respiratory electron transport chain. However, mtROS biology still 440 relies on an eclectic collection of indirect detection techniques, many of which have 441 known shortcomings. A large literature based on mutant studies and transcriptional 442 profiling argues that mtROS represent a hub in a highly interconnected network 443 associated with abiotic stress, defense responses, hormone signalling, intracellular 444 signal transduction, cell death and development in plants. Significant progress has 445 been made in identifying non-mitochondrial components involved in perpetuating 446 putatively mtROS-dependent processes. However, the mitochondrion itself has 447 remained a black box in terms of identifying a sensor or signalling component that 448 can transmit mtROS signals into the cellular ROS network. Future studies will need 449 to consolidate the mtROS literature by using the most appropriate ROS-450 measurement method(s) to answer a specific biological question and provide 451 additional forms of evidence to support the proposed role for mtROS in specific 452 scenarios. These can include: measurement of concomitant alterations in indicators 453 of oxidation such as the redox potential of mitochondrial thiols, physiological 454 parameters associated with mitochondrial respiration such as matrix pH, metabolic 455 products or oxidative modifications of cellular biomolecules; genetic evidence based 456 on targeting appropriate antioxidants or limiting ROS generation systems; and/or 457 analysis of transcriptional responses that overlap with other reports or meta-analyses 458 of oxidative challenge. 459

Key biological questions for the future include: 460

• In which cell types does mtROS-mediated oxidation occur in vivo and what 461 molecules exactly are oxidized by which reactive species? 462

• How do biochemical oxidation mechanisms account for the specificity required 463 for mtROS signalling to be involved in many distinct processes? 464

• What is the physiological and evolutionary significance of the interactions 465 between mtROS and plant hormone signalling? 466

• Do mtROS have a specific role in programmed cell death regulation and 467 pathogen responses in plants? 468

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http://scholar.google.com/scholar?as_q=The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gibala&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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Hoffmann C, Plocharski B, Haferkamp I, Leroch M, Ewald R, Bauwe H, Riemer J, Herrmann JM, Neuhaus HE (2013) Fromendoplasmic reticulum to mitochondria: absence of the Arabidopsis ATP antiporter endoplasmic Reticulum Adenylate Transporter1perturbs photorespiration. Plant Cell 25: 2647-2660


Howell KA, Millar AH, Whelan J (2006) Ordered assembly of mitochondria during rice germination begins with promitochondrialstructures rich in components of the protein import apparatus. Plant molecular biology 60: 201-223


Huang Y, Chen X, Liu Y, Roth C, Copeland C, McFarlane HE, Huang S, Lipka V, Wiermer M, Li X (2013) Mitochondrial AtPAM16 isrequired for plant survival and the negative regulation of plant immunity. Nat Commun 4


Ivanova A, Law SR, Narsai R, Duncan O, Lee J-H, Zhang B, Van Aken O, Radomiljac JD, van der Merwe M, Yi K, et al (2014) AFunctional Antagonistic Relationship between Auxin and Mitochondrial Retrograde Signaling Regulates Alternative Oxidase1aExpression in Arabidopsis. Plant Physiology 165: 1233-1254


Jaipargas EA, Barton KA, Mathur N, Mathur J (2015) Mitochondrial pleomorphy in plant cells is driven by contiguous ER dynamics.Front Plant Sci 6: 783


Jardim-Messeder D, Caverzan A, Rauber R, de Souza Ferreira E, Margis-Pinheiro M, Galina A (2015) Succinate dehydrogenase(mitochondrial complex II) is a source of reactive oxygen species in plants and regulates development and stress responses. NewPhytologist 208: 776-789


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http://search.crossref.org/?page=1&rows=2&q=He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu LJ, Gong Z (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24: 1815-1833

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http://scholar.google.com/scholar?as_q=DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=He&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 25%5BVolume%5D AND 2647%5BPagination%5D AND Hoffmann C%2C Plocharski B%2C Haferkamp I%2C Leroch M%2C Ewald R%2C Bauwe H%2C Riemer J%2C Herrmann JM%2C Neuhaus HE%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hoffmann C, Plocharski B, Haferkamp I, Leroch M, Ewald R, Bauwe H, Riemer J, Herrmann JM, Neuhaus HE (2013) From endoplasmic reticulum to mitochondria: absence of the Arabidopsis ATP antiporter endoplasmic Reticulum Adenylate Transporter1 perturbs photorespiration. Plant Cell 25: 2647-2660

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

http://scholar.google.com/scholar?as_q=From endoplasmic reticulum to mitochondria: absence of the Arabidopsis ATP antiporter endoplasmic Reticulum Adenylate Transporter1 perturbs photorespiration&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=From endoplasmic reticulum to mitochondria: absence of the Arabidopsis ATP antiporter endoplasmic Reticulum Adenylate Transporter1 perturbs photorespiration&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hoffmann&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant molecular biology%5BTitle%5D%29 AND 60%5BVolume%5D AND 201%5BPagination%5D AND Howell KA%2C Millar AH%2C Whelan J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Howell KA, Millar AH, Whelan J (2006) Ordered assembly of mitochondria during rice germination begins with promitochondrial structures rich in components of the protein import apparatus. Plant molecular biology 60: 201-223

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http://scholar.google.com/scholar?as_q=Ordered assembly of mitochondria during rice germination begins with promitochondrial structures rich in components of the protein import apparatus&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Howell&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity%2E%5BTitle%5D%29 AND Huang Y%2C Chen X%2C Liu Y%2C Roth C%2C Copeland C%2C McFarlane HE%2C Huang S%2C Lipka V%2C Wiermer M%2C Li X%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Huang Y, Chen X, Liu Y, Roth C, Copeland C, McFarlane HE, Huang S, Lipka V, Wiermer M, Li X (2013) Mitochondrial AtPAM16 is required for plant survival and the negative regulation of plant immunity. Nat Commun 4

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiology%5BTitle%5D%29 AND 165%5BVolume%5D AND 1233%5BPagination%5D AND Ivanova A%2C Law SR%2C Narsai R%2C Duncan O%2C Lee J%2DH%2C Zhang B%2C Van Aken O%2C Radomiljac JD%2C van der Merwe M%2C Yi K%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ivanova A, Law SR, Narsai R, Duncan O, Lee J-H, Zhang B, Van Aken O, Radomiljac JD, van der Merwe M, Yi K, et al (2014) A Functional Antagonistic Relationship between Auxin and Mitochondrial Retrograde Signaling Regulates Alternative Oxidase1a Expression in Arabidopsis. Plant Physiology 165: 1233-1254

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mitochondrial pleomorphy in plant cells is driven by contiguous ER dynamics%2E%5BTitle%5D%29 AND Jaipargas EA%2C Barton KA%2C Mathur N%2C Mathur J%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Overexpression of ALTERNATIVE OXIDASE1a alleviates mitochondria-dependent programmed cell death induced by aluminium phytotoxicity in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Alternative Oxidase in Resistance to Biotic Stresses: Nicotiana attenuata AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not Manduca sexta Larvae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28The%5BTitle%5D%29 AND 2%5BVolume%5D AND which Affects the Mitochondrial Electron Transport Chain%2C Participates in Multiple Stress and Hormone Responses%2E Molecular Plant 7%3A 290%5BPagination%5D AND Zhu Q%2C Dugardeyn J%2C Zhang C%2C M�hlenbock P%2C Eastmond PJ%2C Valcke R%2C De Coninck B%2C �den S%2C Karampelias M%2C Cammue BPA%2C et al%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Free Radic Biol Med%5BTitle%5D%29 AND 48%5BVolume%5D AND 983%5BPagination%5D AND Zielonka J%2C Kalyanaraman B%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zielonka&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1


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