Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Arabidopsis cysteine-rich trans-membrane module (CYSTM) small proteins play a protective role mainly against heat and UV stresses

Janak Raj Joshi A B , Vikram Singh A and Haya Friedman https://orcid.org/0000-0003-1172-7822 A C
+ Author Affiliations
- Author Affiliations

A Department of Postharvest Science of Fresh Produce, Agricultural Research Organisation (ARO), The Volcani Centre, Bet Dagan, Israel.

B Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Kennedy-Leigh Centre for Horticultural Research, Faculty of Agriculture, Food and Environmental Quality Sciences, Hebrew University of Jerusalem, Rehovot, Israel.

C Corresponding author. Email: hayafr@agri.gov.il.

Functional Plant Biology 47(3) 195-202 https://doi.org/10.1071/FP19236
Submitted: 22 August 2019  Accepted: 15 October 2019   Published: 3 February 2020

Abstract

The genomes of Arabidopsis and other plants contain cysteine-rich small protein of unknown function, harbouring a transmembrane module (CYSTM proteins). In this work we show that the transcript of one gene (At1g05340) encoding a CYSTM protein is induced mainly by heat and to a lesser extent by UV, but less by NaCl or sorbitol. A functional analysis of At1g05340 and its paralog At2g32210 using T-DNA insertional mutants revealed a decrease in seedlings root length, and a lower PSII efficiency in mature plant, due to heat stress and to a lesser extent due to UV stress, in comparison to the effect on wild-type plants. The sensitivity of these mutants to salt or osmotic stresses did not differ from wild type response, indicating a specific function for these genes in heat and UV. Heat and UV increased reactive oxygen species levels in wild type; however, the levels were higher in the mutant line than in wild type due to heat treatment, but was similar in the mutant lines and wild type due to UV stress. Taken together, our results suggest that these small cysteine-rich proteins are necessary for thermotolerance and protection from UV exposure. The proteins encoded by these genes most likely, act in heat stress by reducing reactive oxygen species level by yet unknown mechanism.

Additional keywords: At1g05340, At2g32210, cysteine-rich transmembrane module protein, PSII efficiency, ROS, thermotolerance.


References

Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657.
Genome-wide insertional mutagenesis of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12893945PubMed |

Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiology 141, 311
The roles of reactive oxygen species in plant cells.Crossref | GoogleScholarGoogle Scholar | 16760480PubMed |

Basha E, Lee GJ, Demeler B, Vierling E (2004) Chaperone activity of cytosolic small heat shock proteins from wheat. European Journal of Biochemistry 271, 1426–1436.
Chaperone activity of cytosolic small heat shock proteins from wheat.Crossref | GoogleScholarGoogle Scholar | 15066169PubMed |

Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4, 273
Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops.Crossref | GoogleScholarGoogle Scholar | 23914193PubMed |

Bokszczanin K, Fragkostefanakis S, Bostan H, Bovy A, Chaturvedi P, Chiusano M, Firon N, Iannacone R, Jegadeesan S, Klaczynskid K, Li H, Mariani C, Müller F, Paul P, Paupiere M, Pressman E, Rieu I, Scharf K, Schleiff E, Van Heusden A, Vriezen W, Weckwerth W, Winter P (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Frontiers in Plant Science 4, 315
Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance.Crossref | GoogleScholarGoogle Scholar | 23986766PubMed |

Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Molecular Biology 32, 191–222.
Molecular chaperones and protein folding in plants.Crossref | GoogleScholarGoogle Scholar | 8980480PubMed |

Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. Journal of Experimental Botany 55, 2331–2341.
Genes commonly regulated by water-deficit stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15448178PubMed |

Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90, 856–867.
Reactive oxygen species, abiotic stress and stress combination.Crossref | GoogleScholarGoogle Scholar | 27801967PubMed |

Cui Y, Li M, Yin X, Song S, Xu G, Wang M, Li C, Peng C, Xia X (2018) OsDSSR1, a novel small peptide, enhances drought tolerance in transgenic rice. Plant Science 270, 85–96.
OsDSSR1, a novel small peptide, enhances drought tolerance in transgenic rice.Crossref | GoogleScholarGoogle Scholar | 29576089PubMed |

Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289, 2068–2074.
Climate extremes: observations, modeling, and impacts.Crossref | GoogleScholarGoogle Scholar | 11000103PubMed |

Foyer C, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxidants & Redox Signalling 11, 861–905.
Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications.Crossref | GoogleScholarGoogle Scholar |

Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiology 141, 436–445.
Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16603662PubMed |

Hall AE (2010) Breeding for heat tolerance. In ‘Plant breeding reviews’. pp. 129–168. (John Wiley & Sons, Inc.: Hoboken, NJ, USA)

Heyman J, Canher B, Bisht A, Christiaens F, De Veylder L (2018) Emerging role of the plant ERF transcription factors in coordinating wound defense responses and repair. Journal of Cell Science 131, jcs208215
Emerging role of the plant ERF transcription factors in coordinating wound defense responses and repair.Crossref | GoogleScholarGoogle Scholar | 29242229PubMed |

Inzé A, Vanderauwera S, Hoeberichts FA, Vandorpe M, Van Gaever TIM, Van Breusegem F (2011) A subcellular localization compendium of hydrogen peroxide-induced proteins. Plant, Cell & Environment 35, 308–320.
A subcellular localization compendium of hydrogen peroxide-induced proteins.Crossref | GoogleScholarGoogle Scholar |

Kim K, Portis AR (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Letters 571, 124–128.
Oxygen-dependent H2O2 production by Rubisco.Crossref | GoogleScholarGoogle Scholar | 15280029PubMed |

Matsuo M, Johnson JM, Hieno A, Tokizawa M, Nomoto M, Tada Y, Godfrey R, Obokata J, Sherameti I, Yamamoto YY (2015) High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 levels result in accumulation of reactive oxygen species in Arabidopsis thaliana shoots and roots. Molecular Plant 8, 1253–1273.
High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 levels result in accumulation of reactive oxygen species in Arabidopsis thaliana shoots and roots.Crossref | GoogleScholarGoogle Scholar | 25882345PubMed |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 10938857PubMed |

Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 12234732PubMed |

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
Reactive oxygen gene network of plants.Crossref | GoogleScholarGoogle Scholar | 15465684PubMed |

Møller IM, Sweetlove LJ (2010) ROS signalling – specificity is required. Trends in Plant Science 15, 370–374.
ROS signalling – specificity is required.Crossref | GoogleScholarGoogle Scholar | 20605736PubMed |

Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends in Plant Science 22, 53–65.
Transcriptional regulatory network of plant heat stress response.Crossref | GoogleScholarGoogle Scholar | 27666516PubMed |

Qu A-L, Ding Y-F, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochemical and Biophysical Research Communications 432, 203–207.
Molecular mechanisms of the plant heat stress response.Crossref | GoogleScholarGoogle Scholar | 23395681PubMed |

Rosenwasser S, Rot I, Sollner E, Meyer AJ, Smith Y, Leviatan N, Fluhr R, Friedman H (2011) Organelles contribute differentially to reactive oxygen species-related events during extended darkness. Plant Physiology 156, 185–201.
Organelles contribute differentially to reactive oxygen species-related events during extended darkness.Crossref | GoogleScholarGoogle Scholar | 21372201PubMed |

Rosenwasser S, Fluhr R, Joshi JR, Leviatan N, Sela N, Hetzroni A, Friedman H (2013) ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiology 163, 1071–1083.
ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses.Crossref | GoogleScholarGoogle Scholar | 23922270PubMed |

Rosenwasser S, van Creveld SG, Schatz D, Malitsky S, Tzfadia O, Aharoni A, Levin Y, Gabashvili A, Feldmesser E, Vardi A (2014) Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proceedings of the National Academy of Sciences of the United States of America 111, 2740–2745.
Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment.Crossref | GoogleScholarGoogle Scholar | 24550302PubMed |

Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian Journal of Medical and Biological Research 38, 995–1014.
Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses.Crossref | GoogleScholarGoogle Scholar | 16007271PubMed |

Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high‐salinity stresses using a full‐length cDNA microarray. The Plant Journal 31, 279–292.
Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high‐salinity stresses using a full‐length cDNA microarray.Crossref | GoogleScholarGoogle Scholar | 12164808PubMed |

Sung D-Y, Kaplan F, Lee K-J, Guy CL (2003) Acquired tolerance to temperature extremes. Trends in Plant Science 8, 179–187.
Acquired tolerance to temperature extremes.Crossref | GoogleScholarGoogle Scholar | 12711230PubMed |

Trent JD, Kagawa HK, Paavola CD, McMillan RA, Howard J, Jahnke L, Lavin C, Embaye T, Henze CE (2003) Intracellular localization of a group II chaperonin indicates a membrane-related function. Proceeding of the National Academy of Sciences of the United States of America 100, 15589–15594.
Intracellular localization of a group II chaperonin indicates a membrane-related function.Crossref | GoogleScholarGoogle Scholar |

Venancio TM, Aravind L (2010) CYSTM, a novel cysteine-rich transmembrane module with a role in stress tolerance across eukaryotes. Bioinformatics 26, 149–152.
CYSTM, a novel cysteine-rich transmembrane module with a role in stress tolerance across eukaryotes.Crossref | GoogleScholarGoogle Scholar | 19933165PubMed |

Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
Heat tolerance in plants: an overview.Crossref | GoogleScholarGoogle Scholar |

Xu Y, Yu Z, Zhang D, Huang J, Wu C, Yang G, Yan K, Zhang S, Zheng C (2017) CYSTM, a novel non-secreted cysteine-rich peptide family, involved in environmental stresses in Arabidopsis thaliana. Plant & Cell Physiology 59, 423–438.
CYSTM, a novel non-secreted cysteine-rich peptide family, involved in environmental stresses in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Xu Y, Yu Z, Zhang S, Wu C, Yang G, Yan K, Zheng C, Huang J (2019) CYSTM3 negatively regulates salt stress tolerance in Arabidopsis. Plant Molecular Biology 99, 395–406.
CYSTM3 negatively regulates salt stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30701352PubMed |