The Role of ROS and Redox Signaling During the Initial Cellular Response to Abiotic Stress

Chapter

Abstract

When confronted with abiotic stress, plants actively adjust their metabolism and development. Imbalances in cellular processes are often accompanied by a change in reactive oxygen species (ROS) homeostasis. Uncontrolled accumulation of ROS will result in oxidative damage of plant tissues eventually resulting in cell death. In the last decades, it has become clear that plants exposed to abiotic stress show specific and highly dynamic signaling responses, in which ROS function as genuine signaling molecules. Here, we specifically provide an overview of recent advances and current understanding of the role of ROS signaling during the initial phase of abiotic stress. Although different molecular pathways are involved in the detection of specific forms of abiotic stress, they all share a common basic plan. This includes the production of an oxidative burst, kinase-mediated signal transduction and the activation of dormant transcription factors to initiate transcriptional reprogramming within seconds or minutes of stress detection. In this chapter, the contribution of ROS signaling in the regulation of plant adaptation during high-light, temperature, salt and low-oxygen stress will be addressed.

Keywords

Abiotic stress ROS signal NADPH oxidase Transcriptional regulation Kinase cascade Retrograde signaling 

Abbreviations

Ca2+

Calcium ion

EX

Executer

H2O2

Hydrogen peroxide

·OH

Hydroxyl radicals

mtETC

Mitochondrial electron transport chain

MAPK

Mitogen-activated protein kinase

PRX

Peroxiredoxin

RBOH

Respiratory burst oxidase

ROS

Reactive oxygen species

1O2

Singlet oxygen

SOD

Superoxide dismutase

O2·−

Superoxide

SAA

Systemic acquired acclimation

tAPX

Thylakoid-bound ascorbate peroxidase

Notes

Acknowledgments

The authors wish to thank the RWTH Aachen University for its support.

References

  1. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026–2028CrossRefPubMedGoogle Scholar
  3. Benina M, Ribeiro DM, Gechev TS, Mueller-Roeber B, Schippers JHM (2015) A cell type-specific view on the translation of mRNAs from ROS-responsive genes upon paraquat treatment of Arabidopsis thaliana leaves. Plant, Cell Environ 38:349–363CrossRefPubMedGoogle Scholar
  4. Bjornson M, Benn G, Song X, Comai L, Franz AK, Dandekar AM, Drakakaki G, Dehesh K (2014) Distinct roles for mitogen-activated protein kinase signaling and CALMODULIN-BINDING TRANSCRIPTIONAL ACTIVATOR3 in regulating the peak time and amplitude of the plant general stress response. Plant Physiol 166:988–996CrossRefPubMedPubMedCentralGoogle Scholar
  5. Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Planta 138:447–462CrossRefGoogle Scholar
  6. Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ (2016) Learning the languages of the chloroplast: retrograde signaling and beyond. Annl Rev Plant Biol 67:25–53CrossRefGoogle Scholar
  7. Chang R, Jang CJ, Branco-Price C, Nghiem P, Bailey-Serres J (2012) Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol Biol 78:109–122CrossRefPubMedGoogle Scholar
  8. Choi Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Pro Nat Acad Sci U S A 111:6497–6502CrossRefGoogle Scholar
  9. Delker C, Sonntag L, James GV, Janitza P, Ibañez C, Ziermann H, Peterson T, Denk K, Mull S, Ziegler J, Davis SJ, Schneeberger K, Quint M (2014) The DET1-COP1-HY5 pathway constitutes a multipurpose signaling module regulating plant photomorphogenesis and thermomorphogenesis. Cell Rep 9:1983–1989CrossRefPubMedGoogle Scholar
  10. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dikalov S (2011) Cross talk between mitochondria and NADPH oxidases. Free Rad Biol Med 51:1289–1301CrossRefPubMedPubMedCentralGoogle Scholar
  12. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32:278–289CrossRefPubMedGoogle Scholar
  13. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984CrossRefPubMedPubMedCentralGoogle Scholar
  14. Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: The lingering enigma. Photosynth Res 98:609–620CrossRefPubMedGoogle Scholar
  15. Ensminger I, Busch F, Huner N (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Planta 126:28–44CrossRefGoogle Scholar
  16. Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Döring P, Hirt H (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. Peer J 1:e59CrossRefPubMedPubMedCentralGoogle Scholar
  17. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661CrossRefPubMedGoogle Scholar
  18. Furuya T, Matsuoka D, Nanmori T (2013) Phosphorylation of Arabidopsis thaliana MEKK1 via Ca(2+) signaling as a part of the cold stress response. J Plant Res 126:833–840CrossRefPubMedGoogle Scholar
  19. Furuya T, Matsuoka D, Nanmori T (2014) Membrane rigidification functions upstream of the MEKK1-MKK2-MPK4 cascade during cold acclimation in Arabidopsis thaliana. FEBS Lett 588:2025–2030CrossRefPubMedGoogle Scholar
  20. Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett 582:943–948CrossRefPubMedGoogle Scholar
  21. Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy A, Karpinski S, Mittler R (2016) ROS, calcium and electric signals: Key mediators of rapid systemic signaling in plants. Plant Physiol 171:1606–1615Google Scholar
  22. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1:401–408CrossRefPubMedGoogle Scholar
  23. Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly Sensitive (SOS) pathway: Established and emerging roles. Mol Plant 6:275–286CrossRefPubMedGoogle Scholar
  24. Jiang C, Belfield EJ, Mithani A, Visscher A, Ragoussis J, Mott R, Smith JA, Harberd NP (2012) ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J 31:4359–4370CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jung HS, Crisp PA, Estavillo GM, Cole B, Hong F, Mockler TC, Pogson BJ, Chory J (2013) Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Pro Nat Acad Sci U S A 110:14474–14479CrossRefGoogle Scholar
  26. Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32CrossRefPubMedGoogle Scholar
  27. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K, Herrfurth C, Feussner I, Apel K (2012) Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signalling pathway. Plant Cell 24:3026–3039CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, Shibuya N, Yamane H, Miyao A, Takatsuji H, Takahashi A, Hirochika H (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63:599–612CrossRefPubMedPubMedCentralGoogle Scholar
  29. Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489–503CrossRefPubMedPubMedCentralGoogle Scholar
  30. Krieger-Liszkay A, Trebst A (2006) Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre. J Exp Bot 57:1677–1684CrossRefPubMedGoogle Scholar
  31. Kristiansen KA, Jensen PE, Møller IM, Schulz A (2008) Monitoring reactive oxygen species formation and localization in living cells by use of the fluorescent probe CM-H(2)DCFDA and confocal laser microscopy. Physiol Planta 136:369–383CrossRefGoogle Scholar
  32. Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, Schippers JHM, Dijkwel PP (2012) CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Pro Nat Acad Sci U S A 109:17129–17134CrossRefGoogle Scholar
  33. Langeberg LK, Scott JD (2015) Signalling scaffolds and local organization of cellular behaviour. Nat Rev Mol Cell Biol 16:232–244CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JHM (2014) Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat Comm 5:3767Google Scholar
  35. Macfarlane C, Hansen LD, Florez-Sarasa I, Ribas-Carbo M (2009) Plant mitochondria electron partitioning is independent of short-term temperature changes. Plant, Cell Environ 32:585–591CrossRefGoogle Scholar
  36. Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012) H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287:11717–11729CrossRefPubMedPubMedCentralGoogle Scholar
  37. Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: More than just a classical antioxidant enzyme? Plant Cell Physiol 57:1377–1386PubMedGoogle Scholar
  38. Mehler A (1951) Studies on the reactions of illuminated chloroplasts. Stimulation on inhibition of the reaction with molecular oxygen. Arch Biochem Biophys 34:339–351CrossRefPubMedGoogle Scholar
  39. Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214:775–782CrossRefPubMedGoogle Scholar
  40. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2(84):ra45CrossRefPubMedGoogle Scholar
  41. Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481CrossRefPubMedGoogle Scholar
  42. Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling. J Exp Bot 61:3577–3587CrossRefPubMedGoogle Scholar
  43. Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48CrossRefPubMedGoogle Scholar
  44. Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedPubMedCentralGoogle Scholar
  45. Murata N, Los D (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875–879PubMedPubMedCentralGoogle Scholar
  46. Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20:3148–3162CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H (2006) A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281:38697–38704CrossRefPubMedGoogle Scholar
  48. Nguyen XC, Kim SH, Lee K, Kim KE, Liu XM, Han HJ, Hoang MH, Lee SW, Hong JC, Moon YH, Chung WS (2012) Identification of a C2H2-type zinc finger transcription factor (ZAT10) from Arabidopsis as a substrate of MAP kinase. Plant Cell Rep 31:737–745CrossRefPubMedGoogle Scholar
  49. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pérez-Salamó I, Papdi C, Rigó G, Zsigmond L, Vilela B, Lumbreras V, Nagy I, Horváth B, Domoki M, Darula Z, Medzihradszky K, Bögre L, Koncz C, Szabados L (2014) The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol 165:319–334CrossRefPubMedPubMedCentralGoogle Scholar
  51. Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta 1807:989–998CrossRefPubMedGoogle Scholar
  52. Poyton RO, Ball KA, Castello PR (2009) Mitochondrial generation of free radicals and hypoxic signaling. Trend Endocrinol Metab 20:332–340CrossRefGoogle Scholar
  53. Pucciariello C, Parlanti S, Banti V, Novi G, Perata P (2012) Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol 159:184–196CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat JL, Havaux M (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158:1267–1278CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ramel F, Ksas B, Akkari E, Mialoundama AS, Monnet F, Krieger-Liszkay A, Ravanat JL, Mueller MJ, Bouvier F, Havaux M (2013) Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. Plant Cell 25:1445–1462CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366CrossRefPubMedPubMedCentralGoogle Scholar
  58. Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 278:38921–38925CrossRefPubMedGoogle Scholar
  59. Roach T, Krieger-Liszkay A (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Prot Pept Sci 15:351–362CrossRefGoogle Scholar
  60. Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ, Mewett OP, Howell KA, Whelan J, Kazan K, Pogson BJ (2007) Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19:4091–4110CrossRefPubMedPubMedCentralGoogle Scholar
  61. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21:2829–2843CrossRefPubMedPubMedCentralGoogle Scholar
  62. Santosa IE, Ram PC, Boamfa EI, Laarhoven LJJ, Reuss J, Jackson MB, Harren FJM (2007) Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon. Planta 226:193–202CrossRefPubMedGoogle Scholar
  63. Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119CrossRefPubMedGoogle Scholar
  64. Schippers JHM, Foyer CH, van Dongen JT (2016) Redox regulation in shoot growth, SAM maintenance and flowering. Curr Opin Plant Biol 29:121–128CrossRefPubMedGoogle Scholar
  65. Schippers JHM, Nguyen HM, Lu D, Schmidt R, Mueller-Roeber B (2012) ROS homeostasis during development: an evolutionary conserved strategy. Cell Mol Life Sci 69:3245–3257CrossRefPubMedGoogle Scholar
  66. Schmidt R, Schippers JHM (2015) ROS-mediated redox signaling during cell differentiation in plants. Biochim Biophys Acta 1850:1497–1508CrossRefPubMedGoogle Scholar
  67. Schmidt R, Schippers JHM, Welker A, Mieulet D, Guiderdoni E, Mueller-Roeber B (2012) Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa sp. japonica. AoB Plants 2012:pls011CrossRefPubMedPubMedCentralGoogle Scholar
  68. Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JH, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25:2115–2131CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shumbe L, Chevalier A, Legeret B, Taconnat L, Monnet F, Havaux M (2016) Singlet oxygen-induced cell death in Arabidopsis under high-light stress is controlled by OXI1 kinase. Plant Physiol 170:1757–1771PubMedGoogle Scholar
  70. Singh P, Singha AK (2016) A positive feedback loop governed by SUB1A1 interaction with MITOGEN-ACTIVATED PROTEIN KINASE3 imparts submergence tolerance in rice. Plant Cell 28:1127–43Google Scholar
  71. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699CrossRefPubMedGoogle Scholar
  72. Suzuki N, Devireddy AR, Inupakutika MA, Baxter A, Miller G, Song L, Shulaev E, Azad RK, Shulaev V, Mittler R (2015) Ultra-fast alterations in mRNA levels uncover multiple players in light stress acclimation in plants. Plant J 84:760–772CrossRefPubMedGoogle Scholar
  73. Telfer A, Bishop SM, Phillips D, Barber J (1994) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J Biol Chem 269:13244–13253PubMedGoogle Scholar
  74. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968CrossRefPubMedPubMedCentralGoogle Scholar
  75. van Dongen JT, Licausi F (2015) Oxygen sensing and signaling. Annl Rev Plant Biol 66:345–367CrossRefGoogle Scholar
  76. Voesenek LA, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73CrossRefPubMedGoogle Scholar
  77. Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J, Dietz KJ (2014) Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell 26:1151–65Google Scholar
  78. Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746CrossRefPubMedGoogle Scholar
  79. Waszczak C, Akter S, Eeckhout D, Persiau G, Wahni K, Bodra N, Van Molle I, De Smet B, Vertommen D, Gevaert K, De Jaeger G, Van Montagu M, Messens J, Van Breusegem F (2014) Sulfenome mining in Arabidopsis thaliana. Pro Nat Acad Sci U S A 111:11545–11550CrossRefGoogle Scholar
  80. Willems P, Mhamdi A, Simon S, Storme V, Kerchev PI, Noctor G, Gevaert K, Van Breusegem F (2016) The ROS wheel: refining ROS transcriptional footprints in Arabidopsis. Plant Physiol 171:1720–1733Google Scholar
  81. Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759CrossRefPubMedPubMedCentralGoogle Scholar
  82. Yang CY, Hong CP (2015) The NADPH oxidase RbohD is involved in primary hypoxia signalling and modulates expression of hypoxia-inducible genes under hypoxic stress. Environ Exp Bot 115:63–72CrossRefGoogle Scholar
  83. Yang T, Chaudhuri S, Yang L, Du L, Poovaiah BW (2010a) A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J Biol Chem 285:7119–7126CrossRefPubMedGoogle Scholar
  84. Yang T, Shad Ali G, Yang L, Du L, Reddy AS, Poovaiah BW (2010b) Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal Behav 5:991–994CrossRefPubMedPubMedCentralGoogle Scholar
  85. Yu HD, Yang XF, Chen ST, Wang YT, Li JK, Shen Q, Liu XL, Guo FQ (2012) Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. PLoS Genet 8:e1002669CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zarza X, Atanasov KE, Marco F, Arbona V, Carrasco P, Kopka J, Fotopoulos V, Munnik T, Gómez-Cadenas A, Tiburcio AF, Alcázar R (2016) Polyamine Oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant, Cell Environ. doi: 10.1111/pce.12714 Google Scholar
  87. Zhang S, Apel K, Kim C (2014) Singlet oxygen-mediated and EXECUTER-dependent signalling and acclimation of Arabidopsis thaliana exposed to light stress. Philos Trans Roy Soc Lond B Biol Sci 369:20130227CrossRefGoogle Scholar
  88. Zhang Y, Wang Y, Taylor JL, Jiang Z, Zhang S, Mei F, Wu Y, Wu P, Ni J (2015) Aequorin-based luminescence imaging reveals differential calcium signalling responses to salt and reactive oxygen species in rice roots. J Exp Bot 66:2535–2545CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Institute of Biology IRWTH Aachen UniversityAachenGermany

Personalised recommendations