MITOCH-00889; No of Pages 6 Mitochondrion xxx (2014) xxx–xxx

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Mini-review

Plant mitochondria under a variety of temperature stress conditions Michał Rurek ⁎ Department of Cellular & Molecular Biology, Institute of Molecular Biology & Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznań, Umultowska 89, 61-614 Poznań, Poland

a r t i c l e

i n f o

Article history: Received 13 December 2013 Received in revised form 12 February 2014 Accepted 14 February 2014 Available online xxxx Keywords: Cold stress Heat stress Mitochondrial response Proteome Transcriptome Ultrastructure

a b s t r a c t The biogenesis of plant mitochondria is a multistep process that depends on a concerted expression of mitochondrial and nuclear genes. The balance between different steps of this process, embracing various fluctuations in mitochondrial transcriptome and proteome, may be affected by diverse temperature treatments. A plethora of genes with altered expression during the acting of these stimuli were identified and their expression characterized, including those encoding for classical components of energy dissipating system. Selected aspects of current interest, regarding the functioning of plant mitochondria under cold and heat stresses, are highlighted. © 2014 Elsevier B.V. and Mitochondria Research Society. All rights reserved.

Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Transcriptomic responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Alterations in the mitochondrial proteome and protein import . . . . . . . . . . . . . . . . . 4. Mitochondrial complexome responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Mitochondrial morphology and genome maintenance . . . . . . . . . . . . . . . . . . . . . 6. Mitochondrial metabolism and physiology . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Future directions in the elucidation of plant mitochondrial responses under temperature treatments Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Abiotic stresses, including excessive cold or heat, cause a failure in the cultivation of many plant species, including major crops (Bray et al., 2000). Diverse stress conditions often produce similar effects in

Abbreviations: AOX, alternative oxidase; C(s), complex(es); CSP, cold shock protein; dlps, dehydrin-like proteins; GDC, glycine decarboxylase; COR, cold-regulated; HSPs, heat shock proteins; nat-siRNA, natural antisense transcript-derived small interfering RNA; NDA, internal NAD(P)H dehydrogenases (NDA1 and NDA2); P5CDH, 1Δ-pyrroline5-carboxylate dehydrogenase; PPRs, pentatricopeptide repeat-containing proteins; Pro, proline; ProDH, proline dehydrogenase; PUMP, plant uncoupling mitochondrial protein; SC(s), supercomplex(es); SHMT, serine hydroxymethyltransferase; sHSP(s), small heat shock protein(s); SOD, superoxide dismutase; UCP(s), uncoupling protein(s). ⁎ Tel.: +48 61 8295968; fax: +48 61 8295950. E-mail address: [email protected].

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cellular damage and cellular compartments. Mitochondria are dynamically involved in the stress response (Millar et al., 2005; Taylor et al., 2009), which implies the necessity of coordinated interorganellar communication. Despite their structural variability, plant mitochondrial genomes encode for a limited amount of proteins as numerous mitochondrial genes were shifted to the nuclear genome in the course of evolution (Alverson et al., 2011). Thus, a complicated and multistep biogenesis of plant mitochondria, depending on the concerted expression of mitochondrial and nuclear genes, is indispensable for the correct assembly of protein complexes (Cs) and supercomplexes (SCs); this balance may be affected by environmental stimuli. The adaptation of metabolism to stress in plant mitochondria has been elucidated in its various aspects; nevertheless, the relative importance of that process – at the cellular and physiological levels – may not always be understood properly. Excellent reviews have been published

http://dx.doi.org/10.1016/j.mito.2014.02.007 1567-7249/© 2014 Elsevier B.V. and Mitochondria Research Society. All rights reserved.

Please cite this article as: Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion (2014), http:// dx.doi.org/10.1016/j.mito.2014.02.007

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regarding the functioning of plant mitochondria under selected abiotic stress conditions (Jacoby et al., 2012; Taylor et al., 2009); however, recent data broaden our understanding of plant mitochondrial biogenesis also under temperature stress. The aim of this mini-review is to provide a comprehensive view of selected aspects of mitochondrial functioning and response under cold and heat treatments. 2. Transcriptomic responses During retrograde and anterograde signaling pathways under abiotic stress conditions, the expression of many genes coding for mitochondrial proteins is altered. The heat-associated retrograde response was discovered first in Arabidopsis plants exhibiting increased thermotolerance and super-induced endogenous heat shock protein genes (HSP; reviewed in Rhoads and Subbaiah, 2007). Energy-dissipating components have been postulated to play a key role in the intramitochondrial stress response (Rasmusson et al., 2004) and in active modulation of signaling pathways from mitochondria that could control the cellular stress response (Vanlerberghe et al., 2009). Regulation of diverse AOX (alternative oxidase) genes varies between monocots and dicots. For instance, AOX1a isoform in Arabidopsis is induced under cold and heat stresses (with almost 2-fold change; Elhafez et al., 2006); however, in sugarcane (Saccharum sp.) – during longer chilling – AOX1c is more upregulated (Borecký et al., 2006). Clifton et al. (2005) suggested that the AOX2 isoform plays a role in interorganellar signaling as its transcripts were repressed in stress. Although AOX1 transcripts are generally sensitive to different stress conditions and AOX2 mRNAs are often constitutively synthesized, AOX1d is downregulated during exposure of Arabidopsis plantlets to 4 °C (Borecký and Vercesi, 2005). Interestingly, in Citrus aurantium cold and heat lower AOX mRNA abundance and also strongly suppress the accumulation of internal NAD(P)H dehydrogenase transcripts (Ziogas et al., 2013). Temperature stress alters the amount of mRNAs encoded for uncoupling proteins (UCP1 and UCP2) as well as for most of the investigated alternative NAD(P)H dehydrogenases in Arabidopsis plants; interestingly, NDA1 and NDA2 transcripts encoding for internal NAD(P)H dehydrogenases are reciprocally regulated under cold and heat stresses (Elhafez et al., 2006). The transcriptomic changes inside mitochondria (related to the mRNA turnover and steady-state abundance) are often more evident than proteomic ones (Giegé et al., 2005; Van Aken et al., 2009). Moreover, mRNA levels may not accurately reflect protein abundance, for instance in the case of some HSP genes (Taylor et al., 2009; Van Aken et al., 2009). This implies stress-driven dynamic regulation of the mRNA pool, which is accessible for the synthesis of mitochondrial proteins. Although mitochondrial mRNAs are generally not polyadenylated, the level of poly(A)+ transcripts of mitochondrial origin for mitochondrial genes co-expressed with the heat shock transcription factor At2g26150 is elevated in heat and could be reversed in heat recovery (Adamo et al., 2008). Naydenov et al. (2010), using macroarray analysis and real-time RT-PCR, showed cold-specific alterations of many mitochondrial transcripts in wheat (Triticum aestivum) embryos. It resulted in down- or upregulations in mRNAs of 13 mitochondrial genes. Most of them were downregulated at the initial stage of cold stress, but some (nad, atp and cob) showed a very evident upregulation after 2 or 3 days of cold stress. The levels of some nuclear transcripts (for Mn containing superoxide dismutase [Mn-SOD] and AOX1a) increased. Thus, in wheat embryos the response of mitochondrial transcription during cold stress is very quick in order to postpone embryo development before stress cessation and the occurrence of possible cellular damage. The regulation of Arabidopsis mitochondrial respiratory chain components under temperature stress was also assayed in detail at RNA level by Gonzalez et al. (2007), who noticed a coordinated, tissue- and developmentally-dependent response of mitochondrial Cs components encoded by the nuclear genome. The chilling of Arabidopsis seedlings

resulted in major (N 1.5-fold change) downregulations not only in alternative components of the respiratory chain, but – interestingly – also in γ-carbonic anhydrase isoform and CI and CII subunits. At least 1.5-fold change upregulations were more frequent and comprised 40 alterations, including 25 changes for structural subunits of CI–CIV and ATP synthase. The responses in cold-treated Arabidopsis dry seeds were similar; however, 69 upregulations (N 1.5-fold change) included almost 46 for structural respiratory chain components. 3. Alterations in the mitochondrial proteome and protein import The plant mitochondrial proteome, estimated to comprise at least 1500 proteins (Taylor et al., 2011), is a dynamic structure that responds to genetic, environmental and developmental signals (Millar et al., 2005). Although the amount of low-abundant mitochondrial proteins involved in cold and heat responses is still underestimated (Huang et al., 2011; Taylor et al., 2009), a list of 75 cold- and 51 heat-regulated nonredundant proteins, based on the prominent experimental data, is presented (Supplementary Table 1). However, only a limited number of studies have directly focused on the analysis of the mitochondrial proteome under temperature stress (Qin et al., 2009; Tan et al., 2012; Taylor et al., 2005; Yin et al., 2009). Selected effects of cold and heat stresses on the plant mitochondrial proteome are discussed below. Chilling causes more pronounced breakdown of plant mitochondrial proteins than other stress conditions, like drought, even though drought induces oxidative stress more effectively (Taylor et al., 2005). However, the amount of damaged and modified (for instance oxidized or S-nitrosylated) proteins may increase under cold and – especially – heat stresses. Respiratory chain components are part of such regulation (Ziogas et al., 2013). Diverse effects on mitochondrial protein oxidation under various temperature stress conditions have been reported, even though plastids and peroxisomes in green tissues are the major ROS sources. Mitochondrially-targeted redox-sensitive GFP was significantly oxidized in severe heat. Strikingly, cold impedes perturbations in the mitochondrial redox balance (Schwarzländer et al., 2009). However, the reproducibility of such effects should be validated under field conditions. Diverse dehydrin-like proteins (dlps; 28, 52–63 kDa) were found in the mitochondria of some cereals in cold and frost responses (Borovskii et al., 2002). This study was considerably extended by Rurek (2010), who identified a few novel dlp candidates in yellow lupin (Lupinus luteus), cauliflower (Brassica oleracea var. botrytis) and Arabidopsis mitochondria also under heat stress and heat recovery conditions and specified their submitochondrial localization and topology. Apart from classical heat shock proteins, elevated temperature also stimulates the synthesis of small heat shock proteins (sHSPs; 15–30 kDa) in plant mitochondria (Banzet et al., 1998; Lenne and Douce, 1994; Lund et al., 1998). They protect some respiratory Cs (especially CI — as the most heat-sensitive component of the respiratory chain) from degradation and proteolysis (Downs and Heckathorn, 1998; Lenne and Douce, 1994). In addition, during thermal recovery, proline (Pro) is an important nitrogen or energy resource, a compatible osmolyte and an important ROS scavenger. For its degradation, Pro is imported into mitochondria and converted to glutamate in the Pro/P5C cycle by proline dehydrogenase (ProDH) and 1Δ-pyrroline-5-carboxylate dehydrogenase (P5CDH). Enzymes of the Pro/P5C cycle are frequently expressed in a reciprocal manner under some stress conditions (Peng et al., 1996). Arabidopsis ProDH loss-of-function mutants are sensitive to external proline supply and heat stress (Funck et al., 2010). Free Pro is accumulated in the leaves of cold-treated wild-type cauliflower (B. oleracea var. botrytis) and mutant plants with enhanced frost resistance, selected in hydroxyProcontaining medium (Hadi et al., 2011). The level of mRNA expressed P5CDH significantly decreased in Arabidopsis plants expressing ectopically P5C synthetase 1 under heat stress; Pro accumulation impeded Arabidopsis seedlings growth, which suggests that at least under particular conditions Pro may not serve as an osmolyte (Lv et al., 2011).

Please cite this article as: Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion (2014), http:// dx.doi.org/10.1016/j.mito.2014.02.007

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Although it was shown that various environmental stimuli, including plant chilling, decreased the rate of protein import to plant mitochondria, the processing of imported proteins remains largely unaffected (Taylor et al., 2003). The impact of heat stress on protein import into plant mitochondria still needs to be investigated. 4. Mitochondrial complexome responses The data for the plant mitochondrial complexome showing specific alterations in the level of respiratory Cs and SCs under temperature stress is controversial. The dynamic biogenesis of such large entities might be a part of regulation of electron transfer within respiratory chain components (Bultema et al., 2009). Tan et al. (2012), using a gel-free method, postulated concerted regulation of various mitochondrial proteins in Arabidopsis cell cultures under cold stress, which may theoretically lead to possible changes in Cs abundance. Notably, the dynamic status of respiratory Cs was emphasized by Lenaz and Genova (2012), who suggested that mitochondrial SCs disassembly may occur in the course of oxidative stress. Using conventional BN/SDS-PAGE, Millar et al. (2004) reported a slight increase in the amount of assembled CI and ATP synthase of rice (Oryza sativa) under anoxia recovery and upregulation of a few subunits of CIII and CIV. Furthermore, Ramírez-Aguilar et al. (2011) showed that the stability and activity of large potato (Solanum tuberosum) mitochondrial SCs (containing CI, CIII and CIV at diverse stoichiometry) were altered in long hypoxia. Some mitochondrial Cs, including ATP synthase, are structurally unstable under excessive heat (Heinemeyer et al., 2009). However, direct gel-based evidence for alterations of SCs and Cs abundance under temperature stress and their physiological relevance should be further elaborated. 5. Mitochondrial morphology and genome maintenance Plant mitochondria display size and shape dynamicity controlled by several genes (Logan, 2010). In chilled mung bean (Vigna radiata) suspension cells and in cortical cells of cucumber root tips, extensive mitochondrial swelling was accompanied by some crista swelling during cold recovery (and, in addition, by their disappearance during heat recovery); internal translucence and vesicular structures (Ishikawa, 1996; Lee et al., 2002) were also reported. Under chilling recovery responses of Episcia reptans, mitochondria exhibited disorganization and were visibly burst (Murphy and Wilson, 1981); in addition, Vella et al. (2012) noticed that after prolonged (72 h) chilling in Arabidopsis mesophyll cells, mitochondria were aberrant (also ring-shaped). Contrary to that, a mild heat shock (up to 39 °C) seems to affect no mitochondria in tomato (Lycopersicon esculentum) cell cultures (Neumann et al., 1984); harsher conditions result in mitochondrial membrane swelling, similar to chilling responses. Recently, Wang et al. (2012) showed that heat treatment of tobacco (Nicotiana tabacum) plants extensively enhances the transfer of a few different, variable-length (211–338 bp) mtDNA fragments into the nuclear genome during ds break repair. In addition, the number of mitochondria alongside some dimensions within the plant cell may be slightly altered under cold conditions (as it was reported for Marchantia polymorpha by Ogasawara et al., 2013); however, the relocation of seed plant mitochondria under cold or heat stress needs careful confirmation. 6. Mitochondrial metabolism and physiology Stress conditions regulate plant energetic and metabolic demands, including the ATP/ADP ratio and the need for carbon skeletons inside mitochondria (Millar et al., 2011). Numerous aspects of the plant physiological response to cold and heat stresses have been studied. They are both species- and tissue-specific (Kurimoto et al., 2004; Ribas-Carbo et al., 2000) and also differ between various cultivars of the same species with diverse thermal tolerance (Hu et al., 2010). Photorespiratory

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impairment is often pronounced under temperature stress as glycine decarboxylase (GDC) and serine hydroxymethyltransferase (SHMT) are downregulated (Byun et al., 2009; Taylor et al., 2002, 2005; Xu and Huang, 2010). Low temperature affects mainly mitochondria in the plant cell, changing the respiration rate and activity of CIV and increasing the activity of AOX in non-thermogenic plants, leading to oxidative stress that could be alleviated by AOX while the cytochrome pathway is impaired (Calegario et al., 2003; Sugie et al., 2006). Therefore, the importance of AOX in stress acclimation – including cold acclimation – is suggested (Armstrong et al., 2008; Fiorani et al., 2005). However, AOX is not upregulated under some chilling conditions (Popov et al., 2001). Metabolic variations associated with the AOX level and activity under cold stress were also investigated. Cold-induced AOX aids sugar accumulation in tobacco (N. tabacum) leaves; when the AOX1a isoform is silenced, ROS-scavenging cellular enzymes are increased and lipid peroxidation declines (Wang et al., 2011). The activity of the alternative pathway in cereal plants was elevated preferably during cold hardening and a slight increase of the AOX activity was observed under short cold stress. In pea (Pisum sativum) mitochondria, however, the activity of the alternative pathway was reduced after both treatments (Grabelnych et al., 2004). After a few days of chilling, the total respiration rate together with the alternative pathway activity increased and the cytochrome pathway remained unaffected in cucumber (Cucumis sativus) roots, which thus appeared to be cold tolerant, contrary to the leaves (Hu et al., 2006). Interestingly, Talts et al. (2004) noticed higher rates of dark respiration in cold-acclimated Arabidopsis leaves (with an initial decrease and only a small increase in light respiration after the initial cold shock). The AOX1a overexpression in Arabidopsis leads to constitutive high capacity of the alternative pathway in control and cold-treated plants (Sugie et al., 2006). Uncoupling proteins are also implicated in the temperature stress response. In aox1a knock-out Arabidopsis plants, the expression of UCP1 was cold-increased and associated with novel metabolic balances (Watanabe et al., 2008). In fact, the cold-responsive UCP1 in Arabidopsis leaves keeps the redox poise of the mitochondrial electron transport chain to facilitate photosynthesis (Sweetlove et al., 2006). Cold induces 3 isoforms of plant uncoupling mitochondrial proteins (PUMP1, PUMP4, PUMP5) (Nogueira et al., 2005) and in wheat — CSP 310 protein (cold shock protein containing 55 and 66 kDa subunits), associating with mitochondria under stress conditions (Kolesnichenko et al., 2000); similar proteins were identified in other species (Kolesnichenko et al., 2002). CSP 310 operates under cold stress by shunting electrons from CI to CIV; thus, ubiquinone and CIII bypass occurs (Kolesnichenko et al., 2005). Heat stress can also exert various effects depending on its intensity and duration. It leads to the impairment of the TCA cycle, of the mitochondrial NADH pool, and consequently — of the ATP synthesis. However, it also increases the leaf total respiration as well as the capacities of cytochrome and alternative pathways, and it may be more detrimental to mitochondrial physiology and functioning when accompanied by other stress conditions (Hu et al., 2010). 7. Future directions in the elucidation of plant mitochondrial responses under temperature treatments Based on the discussed data, diverse mitochondrial responses to cold or heat treatments are summarized in Fig. 1. Chilling, cold, freezing and heat stress conditions result in a number of significant structural and physiological changes. Among others, alterations in mitochondrial organization may be accompanied by changes in membrane fluidity and permeability and lipid peroxidation as well as by excessive proteolysis (Taylor et al., 2002, 2005). For instance, freezing causes the formation of an inverted hexagonal phase membrane structure (Sung et al., 2003). Impairment of the efficiency of electron transport within the respiratory chain (related to elevated production of ROS) results in power

Please cite this article as: Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion (2014), http:// dx.doi.org/10.1016/j.mito.2014.02.007

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heteroplasmy affected?

messenger over-accumulation*

mtDNA transfer?

membrane fluidity

CO2

GCS GDC-L

Gly Ser

NAD+

acetyl-CoA SHMT THF

NADH

HSPs

PA

GDC-P GDC-H

PDH

CS

GDC-T 5,10-MTHF

ACON

MDH

TCA

matrix enzyme regulations

FUM

IDH

SDH

OGDC

P5C

ProDHs

Glu

APs

NAD(P)H DHs*

dlps

LPEP

membrane swelling

P5CDH

CIII* CII

novel subunit isoforms?

OM

cytosolic sHSPs oligomerisation

CIV*

AOX UCPs*

ATP synthase NAD(P)H DHs

nuclear-encoded mt proteins

ROS

sHSPs

IM IMS

general and carrier import protein PTMs & proteases pathways oxidative damage affected

SCL

Pro catabolism Pro

NUCLEUS

OM Cs with CSP310*

dehydrins

SCs assembly/ disassembly?

Fig. 1. Various responses to temperature stress that alter plant mitochondrial biogenesis. Only most relevant processes are shown. Phenomena and proteins postulated to be involved in cold and heat response that need further experimental evidences are indicated by a question mark (?) and the chosen ones involved in cold/heat recovery — by asterisks (*). Various posttranslational protein modifications (PTMs) are depicted by small black and gray dots on proteins in the upper panel (protein PTMs & oxidative damage). In matrix enzyme panel the oval intensity for each protein is proportional to its participation in thermal stress response among analyzed species (based on Supplementary Table 1). For more details — see text. Further abbreviations: ACON — aconitase; AOX — alternative oxidase; APs — antioxidant protein system; C(s) — complex(es); CS — citrate synthase; CSP — cold shock protein; DHs — alternative NAD(P)H dehydrogenase; dlps — dehydrin-like proteins; FUM — fumarase; GCS — glycine cleavage system; GDC — glycine decarboxylase; Gly — glycine; Glu — glutamate; HSPs — heatshock proteins; IDH — isocitrate dehydrogenase; IM — inner membrane; IMS — intermembrane space; LPEP — lipid peroxidation products; MDH — malate dehydrogenase; mt — mitochondrial; MTHF — N5,N10-methylene-tetrahydrofolate; OGDC — 2-oxoglutarate dehydrogenase; OM — outer membrane; P5CDH — 1Δ-pyrroline-5-carboxylate dehydrogenase; PA — pyruvic acid; PDH — pyruvate dehydrogenase; Pro — proline; ProDHs — proline dehydrogenases; ROS — reactive oxygen species; SCs — supercomplexes; SCL — succinyl-CoA synthase; SDH — succinate dehydrogenase; Ser — serine; SHMT — serine hydroxymethyltransferase; sHSPs — small heat shock proteins; TCA — tricarboxylic acid cycle; THF — tetrahydrofolate; UCPs — uncoupling proteins.

and energy production deficiencies (Foyer and Noctor, 2009). Besides the oxidative burst, dehydration is also a common phenomenon for diverse temperature stress conditions (Borovskii et al., 2002; Rurek, 2010). A severe decrease in the respiration rate and photosynthetic activity, despite the compensatory activities of photorespiratory and TCA enzymes, leads to decreased plant productivity (Barnabás et al., 2008). These impairments can be mediated through the kinetic effects of electron transport (Armstrong et al., 2008). In particular, temperature stress may result in premature plant senescence, programmed cell death and male sterility accompanied by mitochondrial alterations (Rikhvanov et al., 2007; Sakata et al., 2010). Plant mitochondria are also involved in the regulation of cellular Ca 2 + homeostasis; moreover, they participate in anterograde and retrograde signaling. During such responses multiple pathways acting within plant cells are also altered, especially that the production of key phytohormones (including ABA, salicylic acid and ethylene) increases under temperature treatments (Larkindale et al., 2005). Overall, a complex interplay between mitochondria and other cellular components occurs under various thermal treatments. However, some unclear points in our understanding of how plant mitochondria function under cold and heat remain to be clarified. First, numerous analyses of mitochondrial functioning at low and high temperatures were carried out applying stress treatments under laboratory conditions including environmental chambers. It would be

interesting to verify those results also in the field, whenever possible. In particular, the influence of temperature stress on mitochondrial heteroplasmy and nuclear mitochondrial DNA dynamics during crop cultivation is worth elaborating. It is tempting to determine to what extent small regulatory RNAs can influence mitochondrial biogenesis in cold and heat. Initially, natural antisense transcript-derived small interfering RNAs (nat-siRNAs) were discovered. They regulate P5CDH gene expression, leading to Pro overaccumulation under salinity (Borsani et al., 2005). In addition, a specific microRNA (miR398) interacts with transcripts encoding SOD isoforms induced by abiotic stresses (Sunkar et al., 2006). Hypoxia-responsive small RNAs target some mitochondrially-predicted pentatricopeptide repeat-containing proteins (PPRs) (Moldovan et al., 2010); are such interactions important in cold and heat response? Another question is: are many activities involving PPRs and other RNA editing factors altered under such conditions (Zhu et al., 2014)? As regards the proteome level, as the coordination of assembly/ disassembly of plant mitochondrial SCs and Cs seems to be a crucial step for mitochondrial biogenesis at least under certain treatments (Giegé et al., 2005), further research should focus on the analysis of potential stoichiometric alterations in plant mitochondrial complexome (Tan et al., 2012) including low-abundant Cs under cold and heat conditions. Relevant physiological consequences of such changes should be discussed. Analyses of alterations in protein posttranslational

Please cite this article as: Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion (2014), http:// dx.doi.org/10.1016/j.mito.2014.02.007

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modifications under cold and heat stresses are also necessary in order to better understand mitochondrial biogenesis under such conditions. Finally, all studies are expected to be accompanied by more metabolic and fluxomic data (Sweetlove et al., 2002). Furthermore, new research should focus on collecting mitochondrial response data under combined temperature and other stress treatments. Such approach will allow understanding of those processes in a broader biological context. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.mito.2014.02.007. Conflict of interest The author declares no conflict of interests. Acknowledgments This work was supported by the resources for science provided by the Ministry of Science and Higher Education, Poland, grant no. N N303 338835 (to M.R.) and by OPUS grant no. 2011/03/B/NZ9/05237 of the National Science Centre, Poland. References Adamo, A., Pinney, J.W., Kunova, A., Westhead, D.R., Meyer, P., 2008. Heat stress enhances the accumulation of polyadenylated mitochondrial transcripts in Arabidopsis thaliana. PLoS One 3, e2889. Alverson, A.J., Rice, D.W., Dickinson, S., Barry, K., Palmer, J.D., 2011. Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23, 2499–2513. Armstrong, A.F., Badger, M.R., Day, D.A., Barthet, M.M., Smith, P.M.C., Millar, A.H., Whelan, J., Atkin, O.K., 2008. Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. Plant Cell Environ. 31, 1156–1169. Banzet, N., Richaud, C., Deveaux, Y., Kazmaier, M., Gagnon, J., Triantaphylidès, C., 1998. Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J. 13, 519–527. Barnabás, B., Jäger, K., Fehér, A., 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 31, 11–38. Borecký, J., Vercesi, A.E., 2005. Plant uncoupling mitochondrial protein and alternative oxidase: energy metabolism and stress. Biosci. Rep. 25, 271–286. Borecký, J., Nogueira, F.T.S., de Oliveira, K.A.P., Maia, I.G., Vercesi, A.E., Arruda, P., 2006. The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots. J. Exp. Bot. 57, 849–864. Borovskii, G.B., Stupnikova, I.V., Antipina, A.I., Vladimirova, S.V., Voinikov, V.K., 2002. Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol. 2, 5. Borsani, O., Zhu, J., Verslues, P.E., Sunkar, R., Zhu, J.-K., 2005. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123, 1279–1291. Bray, E.A., Bailey-Serres, J., Weretilnyk, E., 2000. Responses to abiotic stresses. In: Gruissem, W., Buchannan, B., Jones, R. (Eds.), Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, pp. 158–1249. Bultema, J.B., Braun, H.-P., Boekema, E.J., Kouril, R., 2009. Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochim. Biophys. Acta 1787, 60–67. Byun, Y.-J., Kim, H.-J., Lee, D.-H., 2009. LongSAGE analysis of the early response to cold stress in Arabidopsis leaf. Planta 229, 1181–1200. Calegario, F.F., Cosso, R.G., Fagian, M.M., Almeida, F.V., Jardim, W.F., Jezek, P., Arruda, P., Vercesi, A.E., 2003. Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase. J. Bioenerg. Biomembr. 35, 211–220. Clifton, R., Lister, R., Parker, K.L., Sappl, P.G., Elhafez, D., Millar, A.H., Day, D.A., Whelan, J., 2005. Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193–212. Downs, C.A., Heckathorn, S.A., 1998. The mitochondrial small heat-shock protein protects NADH:ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. FEBS Lett. 430, 246–250. Elhafez, D., Murcha, M.W., Clifton, R., Soole, K.L., Day, D.A., Whelan, J., 2006. Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol. 47, 43–54. Fiorani, F., Umbach, A.L., Siedow, J.N., 2005. The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol. 139, 1795–1805. Foyer, C.H., Noctor, G., 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861–905. Funck, D., Eckard, S., Müller, G., 2010. Non-redundant functions of two proline dehydrogenase isoforms in Arabidopsis. BMC Plant Biol. 10, 70.

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Giegé, P., Sweetlove, L.J., Cognat, V., Leaver, C.J., 2005. Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17, 1497–1512. Gonzalez, D.H., Welchen, E., Attallah, C.V., Comelli, R.N., Mufarrege, E.F., 2007. Transcriptional coordination of the biogenesis of the oxidative phosphorylation machinery in plants. Plant J. 51, 105–116. Grabelnych, O.I., Sumina, O.N., Funderat, S.P., Pobezhimova, T.P., Voinikov, V.K., Kolesnichenko, A.V., 2004. The distribution of electron transport between the main cytochrome and alternative pathways in plant mitochondria during short-term cold stress and cold hardening. J. Therm. Biol. 29, 165–175. Hadi, F., Gilpin, M., Fuller, M.P., 2011. Identification and expression analysis of CBF/DREB1 and COR15 genes in mutants of Brassica oleracea var. botrytis with enhanced proline production and frost resistance. Plant Physiol. Biochem. 49, 1323–1332. Heinemeyer, J., Scheibe, B., Schmitz, U.K., Braun, H.-P., 2009. Blue native DIGE as a tool for comparative analyses of protein complexes. J. Proteome 72, 539–544. Hu, W.H., Shi, K., Song, X.S., Xia, X.J., Zhou, Y.H., Yu, J.Q., 2006. Different effects of chilling on respiration in leaves and roots of cucumber (Cucumis sativus). Plant Physiol. Biochem. 44, 837–843. Hu, W.H., Xiao, Y.A., Zeng, J.J., Hu, X.H., 2010. Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses. Biol. Plant. 54, 761–765. Huang, S.A., Millar, A.H., Taylor, N.L., 2011. The plant mitochondrial proteome composition and stress response: conservation and divergence between monocots and dicots. In: Kempken, F. (Ed.), Plant Mitochondria, Advances in Plant Biology 1. Springer Science + Business Media. Ishikawa, H., 1996. Ultrastructural features of chilling injury: injured cells and the early events during chilling of suspension-cultured mung bean cells. Am. J. Bot. 83, 825–835. Jacoby, R.P., Li, L., Huang, S., Pong Lee, C., Millar, A.H., Taylor, N.L., 2012. Mitochondrial composition, function and stress response in plants. J. Integr. Plant Biol. 54, 887–906. Kolesnichenko, A.V., Grabelnych, O.I., Pobezhimova, T.P., Voinikov, V.K., 2000. The association of plant stress uncoupling protein CSP 310 with winter wheat mitochondria in vitro during exposure to low temperature. J. Plant Physiol. 156, 805–807. Kolesnichenko, A.V., Pobezhimova, T.P., Grabelnych, O.I., Voinikov, V.K., 2002. Stressinduced protein CSP 310: a third uncoupling system in plants. Planta 215, 279–286. Kolesnichenko, A.V., Grabelnych, O.I., Pobezhimova, T.P., Voinikov, V.K., 2005. Nonphosphorylating bypass of the plant mitochondrial respiratory chain by stress protein CSP 310. Planta 221, 113–122. Kurimoto, K., Millar, A.H., Lambers, H., Day, D.A., Noguchi, K., 2004. Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant Cell Physiol. 45, 1015–1022. Larkindale, J., Hall, J.D., Knight, M.R., Vierling, E., 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882–897. Lee, S.H., Singh, A.P., Chung, G.C., Kim, Y.S., Kong, I.B., 2002. Chilling root temperature causes rapid ultrastructural changes in cortical cells of cucumber (Cucumis sativus L.) root tips. J. Exp. Bot. 53, 2225–2237. Lenaz, G., Genova, M.L., 2012. Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation. Adv. Exp. Med. Biol. 748, 107–144. Lenne, C., Douce, R., 1994. A low molecular mass heat-shock protein is localized to higher plant mitochondria. Plant Physiol. 105, 1255–1261. Logan, D.C., 2010. Mitochondrial fusion, division and positioning in plants. Biochem. Soc. Trans. 38, 789–795. Lund, A.A., Blum, P.H., Bhattramakki, D., Elthon, T.E., 1998. Heat-stress response of maize mitochondria. Plant Physiol. 116, 1097–1110. Lv, W.-T., Lin, B., Zhang, M., Hua, X.-J., 2011. Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol. 156, 1921–1933. Millar, A.H., Trend, A.E., Heazlewood, J.L., 2004. Changes in the mitochondrial proteome during the anoxia to air transition in rice focus around cytochrome-containing respiratory complexes. J. Biol. Chem. 279, 39471–39478. Millar, A.H., Heazlewood, J.L., Kristensen, B.K., Braun, H.-P., Møller, I.M., 2005. The plant mitochondrial proteome. Trends Plant Sci. 10, 36–43. Millar, A.H., Whelan, J., Soole, K.L., Day, D.A., 2011. Organization and regulation of mitochondrial respiration in plants. Annu. Rev. Plant Biol. 62, 79–104. Moldovan, D., Spriggs, A., Yang, J., Pogson, B.J., Dennis, E.S., Wilson, I.W., 2010. Hypoxiaresponsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J. Exp. Bot. 61, 165–177. Murphy, C., Wilson, J.M., 1981. Ultrastructural features of chilling-injury in Episcia reptans. Plant Cell Environ. 4, 261–265. Naydenov, N.G., Khanam, S., Siniauskaya, M., Nakamura, C., 2010. Profiling of mitochondrial transcriptome in germinating wheat embryos and seedlings subjected to cold, salinity and osmotic stresses. Genes Genet. Syst. 85, 31–42. Neumann, D., Scharf, K.D., Nover, L., 1984. Heat shock induced changes of plant cell ultrastructure and autoradiographic localization of heat shock proteins. Eur. J. Cell Biol. 34, 254–264. Nogueira, F.T.S., Borecký, J., Vercesi, A.E., Arruda, P., 2005. Genomic structure and regulation of mitochondrial uncoupling protein genes in mammals and plants. Biosci. Rep. 25, 209–226. Ogasawara, Y., Ishizaki, K., Kohchi, T., Kodama, Y., 2013. Cold-induced organelle relocation in the liverwort Marchantia polymorpha L. Plant Cell Environ. 36, 1520–1528. Peng, Z., Lu, Q., Verma, D.P., 1996. Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol. Gen. Genet. 253, 334–341. Popov, V.N., Purvis, A.C., Skulachev, V.P., Wagner, A.M., 2001. Stress-induced changes in ubiquinone concentration and alternative oxidase in plant mitochondria. Biosci. Rep. 21, 369–379.

Please cite this article as: Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion (2014), http:// dx.doi.org/10.1016/j.mito.2014.02.007

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M. Rurek / Mitochondrion xxx (2014) xxx–xxx

Qin, G., Meng, X., Wang, Q., Tian, S., 2009. Oxidative damage of mitochondrial proteins contributes to fruit senescence: a redox proteomics analysis. J. Proteome Res. 8, 2449–2462. Ramírez-Aguilar, S.J., Keuthe, M., Rocha, M., Fedyaev, V.V., Kramp, K., Gupta, K.J., Rasmusson, A.G., Schulze, W.X., van Dongen, J.T., 2011. The composition of plant mitochondrial supercomplexes changes with oxygen availability. J. Biol. Chem. 286, 43045–43053. Rasmusson, A.G., Soole, K.L., Elthon, T.E., 2004. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu. Rev. Plant Biol. 55, 23–39. Rhoads, D.M., Subbaiah, C.C., 2007. Mitochondrial retrograde regulation in plants. Mitochondrion 7, 177–194. Ribas-Carbo, M., Aroca, R., Gonzàlez-Meler, M.A., Irigoyen, J.J., Sánchez-Díaz, M., 2000. The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiol. 122, 199–204. Rikhvanov, E.G., Gamburg, K.Z., Varakina, N.N., Rusaleva, T.M., Fedoseeva, I.V., Tauson, E.L., Stupnikova, I.V., Stepanov, A.V., Borovskii, G.B., Voinikov, V.K., 2007. Nuclearmitochondrial cross-talk during heat shock in Arabidopsis cell culture. Plant J. 52, 763–778. Rurek, M., 2010. Diverse accumulation of several dehydrin-like proteins in cauliflower (Brassica oleracea var. botrytis), Arabidopsis thaliana and yellow lupin (Lupinus luteus) mitochondria under cold and heat stress. BMC Plant Biol. 10, 181. Sakata, T., Oshino, T., Miura, S., Tomabechi, M., Tsunaga, Y., Higashitani, N., Miyazawa, Y., Takahashi, H., Watanabe, M., Higashitani, A., 2010. Auxins reverse plant male sterility caused by high temperatures. Proc. Natl. Acad. Sci. U. S. A. 107, 8569–8574. Schwarzländer, M., Fricker, M.D., Sweetlove, L.J., 2009. Monitoring the in vivo redox state of plant mitochondria: effect of respiratory inhibitors, abiotic stress and assessment of recovery from oxidative challenge. Biochim. Biophys. Acta 1787, 468–475. Sugie, A., Naydenov, N., Mizuno, N., Nakamura, C., Takumi, S., 2006. Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet. Syst. 81, 349–354. Sung, D.-Y., Kaplan, F., Lee, K.-J., Guy, C.L., 2003. Acquired tolerance to temperature extremes. Trends Plant Sci. 8, 179–187. Sunkar, R., Kapoor, A., Zhu, J.-K., 2006. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18, 2051–2065. Sweetlove, L.J., Heazlewood, J.L., Herald, V., Holtzapffel, R., Day, D.A., Leaver, C.J., Millar, A.H., 2002. The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32, 891–904. Sweetlove, L.J., Lytovchenko, A., Morgan, M., Nunes-Nesi, A., Taylor, N.L., Baxter, C.J., Eickmeier, I., Fernie, A.R., 2006. Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 103, 19587–19592. Talts, P., Pärnik, T., Gardeström, P., Keerberg, O., 2004. Respiratory acclimation in Arabidopsis thaliana leaves at low temperature. J. Plant Physiol. 161, 573–579. Tan, Y.-F., Millar, A.H., Taylor, N.L., 2012. Components of mitochondrial oxidative phosphorylation vary in abundance following exposure to cold and chemical stresses. J. Proteome Res. 11, 3860–3879.

Taylor, N.L., Day, D.A., Millar, A.H., 2002. Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J. Biol. Chem. 277, 42663–42668. Taylor, N.L., Rudhe, C., Hulett, J.M., Lithgow, T., Glaser, E., Day, D.A., Millar, A.H., Whelan, J., 2003. Environmental stresses inhibit and stimulate different protein import pathways in plant mitochondria. FEBS Lett. 547, 125–130. Taylor, N.L., Heazlewood, J.L., Day, D.A., Millar, A.H., 2005. Differential impact of environmental stresses on the pea mitochondrial proteome. Mol. Cell. Proteomics 4, 1122–1133. Taylor, N.L., Tan, Y.-F., Jacoby, R.P., Millar, A.H., 2009. Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J. Proteome 72, 367–378. Taylor, N.L., Heazlewood, J.L., Millar, A.H., 2011. The Arabidopsis thaliana 2-D gel mitochondrial proteome: refining the value of reference maps for assessing protein abundance, contaminants and post-translational modifications. Proteomics 11, 1720–1733. Van Aken, O., Zhang, B., Carrie, C., Uggalla, V., Paynter, E., Giraud, E., Whelan, J., 2009. Defining the mitochondrial stress response in Arabidopsis thaliana. Mol. Plant 2, 1310–1324. Vanlerberghe, G.C., Cvetkovska, M., Wang, J., 2009. Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol. Plant. 137, 392–406. Vella, N.G.F., Joss, T.V., Roberts, T.H., 2012. Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming. Protoplasma 249, 1137–1149. Wang, J., Rajakulendran, N., Amirsadeghi, S., Vanlerberghe, G.C., 2011. Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol. Plant. 142, 339–351. Wang, D., Lloyd, A.H., Timmis, J.N., 2012. Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants. Proc. Natl. Acad. Sci. U. S. A. 109, 2444–2448. Watanabe, C.K., Hachiya, T., Terashima, I., Noguchi, K., 2008. The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defence systems in Arabidopsis thaliana leaves. Plant Cell Environ. 31, 1190–1202. Xu, C., Huang, B., 2010. Differential proteomic response to heat stress in thermal Agrostis scabra and heat-sensitive Agrostis stolonifera. Physiol. Plant. 139, 192–204. Yin, G., Sun, H., Xin, X., Qin, G., Liang, Z., Jing, X., 2009. Mitochondrial damage in the soybean seed axis during imbibition at chilling temperatures. Plant Cell Physiol. 50, 1305–1318. Zhu, Q., Dugardeyn, J., Zhang, C., Mühlenbock, P., Eastmond, P.J., Valcke, R., De Coninck, B., Oden, S., Karampelias, M., Cammue, B.P.A., Prinsen, E., Van Der Straeten, D., 2014. The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses. Mol. Plant 7, 290–310. Ziogas, V., Tanou, G., Filippou, P., Diamantidis, G., Vasilakakis, M., Fotopoulos, V., Molassiotis, A., 2013. Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol. Biochem. 68, 118–126.

Please cite this article as: Rurek, M., Plant mitochondria under a variety of temperature stress conditions, Mitochondrion (2014), http:// dx.doi.org/10.1016/j.mito.2014.02.007