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Role of ethylene biosynthesis and signaling in elevated CO2-induced heat stress response in tomato

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Abstract

Main conclusion

This article unveiled that ethylene biosynthesis and signaling play a critical role in heat stress response of tomato plants under elevated CO2.

Abstract

Plant responses to elevated CO2 and heat stress are tightly regulated by an intricate network of phytohormones. Plants accumulate ethylene (ET), the smallest hormone, in response to heat stress; however, the role of ET and its signaling in elevated CO2-induced heat stress response remains largely unknown. In this study, we found that transcript levels of multiple genes relating to ET synthesis, signaling, and heat shock proteins (HSPs) were induced by elevated CO2 (800 μmol mol−1) compared to ambient CO2 (400 μmol mol−1) in tomato leaves under controlled temperature conditions (25 °C). Elevated CO2-induced responses to heat stress (42 °C) were closely associated with increased ET production and HSP70 expression at both transcript and protein levels. Pretreatment with an antagonist of ET, 1-methylcyclopropene that inhibits ET-dependent responses, abolished elevated CO2-induced stress response without affecting the ET production rate. In addition, silencing of ethylene response factor 1 (ERF1) compromised elevated CO2-induced responses to heat stress, which was associated with the concomitant reduction in the transcript of heat shock factor A2, HSP70 and HSP90, indicating that ERF1 is required for elevated CO2-induced responses to heat. All these results provide convincing evidence on the importance of ET biosynthesis and signaling in elevated CO2-induced heat stress response in tomato plants. Thus, the study advances our understanding of the mechanisms of elevated CO2-induced stress response and may potentially be useful for breeding heat-tolerant tomatoes in the era of climate change.

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Abbreviations

1-MCP:

1-Methylcyclopropene

ACO:

ACC oxidases

ERFs:

Ethylene response factors

ET:

Ethylene

HSFs:

Heat shock factors

HSPs:

Heat shock proteins

REC:

Relative electrical conductivity

VIGS:

Virus-induced gene silencing

References

  • Ahammed GJ, Li X, Yu J, Shi K (2015) NPR1-dependent salicylic acid signaling is not involved in elevated CO2-induced heat stress tolerance in Arabidopsis thaliana. Plant Signal Behav 10(6):e1011944

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blankenship SM, Dole JM (2003) 1-Methylcyclopropene: a review. Postharvest Biol Technol 28(1):1–25

    Article  CAS  Google Scholar 

  • Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162(3):1566–1582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cottee NS, Wilson IW, Tan DKY, Bange MP (2014) Understanding the molecular events underpinning cultivar differences in the physiological performance and heat tolerance of cotton (Gossypium hirsutum). Funct Plant Biol 41(1):56–67

    Article  CAS  Google Scholar 

  • Dal Cin V, Rizzini FM, Botton A, Tonutti P (2006) The ethylene biosynthetic and signal transduction pathways are differently affected by 1-MCP in apple and peach fruit. Postharvest Biol Technol 42:125–133

    Article  CAS  Google Scholar 

  • Ding X, Zhu X, Ye L, Xiao S, Wu Z, Chen W, Li X (2019) The interaction of CpEBF1 with CpMADSs is involved in cell wall degradation during papaya fruit ripening. Hortic Res 6:13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7(1):40–49

    Article  PubMed  CAS  Google Scholar 

  • Erpen L, Devi HS, Grosser JW, Dutt M (2017) Potential use of the DREB/ERF, MYB, NAC and WRKY transcription factors to improve abiotic and biotic stress in transgenic plants. Plant Cell Tissue Organ Cult 132(1):1–25

    Article  CAS  Google Scholar 

  • Firon N, Pressman E, Meir S, Khoury R, Altahan L (2012) Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants. https://doi.org/10.1093/aobpla/pls024

    Article  PubMed  PubMed Central  Google Scholar 

  • Fragkostefanakis S, Mesihovic A, Simm S, Paupiere MJ, Hu Y, Paul P, Mishra SK, Tschiersch B, Theres K, Bovy A, Schleiff E, Scharf KD (2016) HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol 170(4):2461–2477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Sun Y, Li Y, Liu X, Zhang W, Ge F (2014) Elevated CO2 decreases the response of the ethylene signaling pathway in Medicago truncatula and increases the abundance of the pea aphid. New Phytol 201(1):279–291

    Article  CAS  PubMed  Google Scholar 

  • Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23(2):741–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Sci 172(6):1113–1123

    Article  CAS  Google Scholar 

  • Huang L, Ren Q, Sun Y, Ye L, Cao H, Ge F (2012) Lower incidence and severity of tomato virus in elevated CO2 is accompanied by modulated plant induced defence in tomato. Plant Biol 14(6):905–913

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2014) Climate Change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Cambridge University Press, Geneva

    Google Scholar 

  • Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J 15(4):405–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jegadeesan S, Beery A, Altahan L, Meir S, Pressman E, Firon N (2018) Ethylene production and signaling in tomato (Solanum lycopersicum) pollen grains is responsive to heat stress conditions. Plant Reprod 31(4):367–383

    Article  CAS  PubMed  Google Scholar 

  • Klay I, Gouia S, Liu M, Mila I, Khoudi H, Bernadac A, Bouzayen M, Pirrello J (2018) Ethylene Response Factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Sci 274:137–145

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Doering P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10(3):310–316

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Huang BR (2005) Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul 47(1):17–28

    Article  CAS  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128(2):682–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Liu SS, Yi CY, Wang F, Zhou J, Xia XJ, Shi K, Zhou YH, Yu JQ (2014) Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant Cell Environ 37(12):2768–2780

    Article  CAS  PubMed  Google Scholar 

  • Li X, Ahammed GJ, Zhang YQ, Zhang GQ, Sun ZH, Zhou J, Zhou YH, Xia XJ, Yu JQ, Shi K (2015) Carbon dioxide enrichment alleviates heat stress by improving cellular redox homeostasis through an ABA-independent process in tomato plants. Plant Biol 17(1):81–89

    Article  CAS  PubMed  Google Scholar 

  • Li XD, Wang XL, Cai YM, Wu JH, Mo BT, Yu ER (2017) Arabidopsis heat stress transcription factors A2 (HSFA2) and A3 (HSFA3) function in the same heat regulation pathway. Acta Physiol Plant 39(3):67

    Article  CAS  Google Scholar 

  • Li X, Zhang L, Ahammed GJ, Li YT, Wei JP, Yan P, Zhang LP, Han X, Han WY (2018) Salicylic acid acts upstream of nitric oxide in elevated carbon dioxide-induced flavonoid biosynthesis in tea plant (Camellia sinensis L.). Environ Exp Bot 161:367–374. https://doi.org/10.1016/j.envexpbot.2018.11.012

    Article  CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazorra LM, Holton N, Bishop GJ, Nunez M (2011) Heat shock response in tomato brassinosteroid mutants indicates that thermotolerance is independent of brassinosteroid homeostasis. Plant Physiol Biochem 49:1420–1428

    Article  CAS  PubMed  Google Scholar 

  • Mullins ED, McCollum TG, McDonald RE (2000) Consequences on ethylene metabolism of inactivating the ethylene receptor sites in diseased non-climacteric fruit. Postharvest Biol Technol 19:155–164

    Article  CAS  Google Scholar 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22(1):53–65

    Article  CAS  PubMed  Google Scholar 

  • Pan C, Ahammed GJ, Li X, Shi K (2018) Elevated CO2 improves photosynthesis under high temperature by attenuating the functional limitations to energy fluxes, electron transport and redox homeostasis in tomato leaves. Front Plant Sci 9:1739

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruggieri V, Calafiore R, Schettini C, Rigano M, Olivieri F, Frusciante L, Barone A (2019) Exploiting genetic and genomic resources to enhance heat-tolerance in tomatoes. Agronomy 9(1):22

    Article  Google Scholar 

  • Shi K, Li X, Zhang H, Zhang GQ, Liu YR, Zhou YH, Xia XJ, Chen ZX, Yu JQ (2015) Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2-induced stomatal movement in tomato. New Phytol 208(2):342–353

    Article  CAS  PubMed  Google Scholar 

  • Song L, Jiang Y, Zhao H, Hou M (2012) Acquired thermotolerance in plants. Plant Cell Tissue Organ Cult 111(3):265–276

    Article  CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126(1):45–51

    Article  CAS  Google Scholar 

  • Torres CA, Sepulveda G, Kahlaoui B (2017) Phytohormone interaction modulating fruit responses to photooxidative and heat stress on apple (Malus domestica Borkh.). Front Plant Sci 8:2129

    Article  PubMed  PubMed Central  Google Scholar 

  • Vankooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25(3):147–150

    Article  CAS  Google Scholar 

  • Wang Y, Du ST, Li LL, Huang LD, Fang P, Lin XY, Zhang YS, Wang HL (2009) Effect of CO2 elevation on root growth and its relationship with indole acetic acid and ethylene in tomato seedlings. Pedosphere 19(5):570–576

    Article  CAS  Google Scholar 

  • Wang D, Heckathorn SA, Hamilton EW, Frantz J (2014) Effects of CO2 on the tolerance of photosynthesis to heat stress can be affected by photosynthetic pathway and nitrogen. Am J Bot 101(1):34–44

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Cai SY, Yin LL, Shi K, Xia XJ, Zhou YH, Yu JQ, Zhou J (2015) Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 11(11):2033–2047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XL, Qin RR, Sun RH, Wang JJ, Hou XG, Qi L, Shi J, Li XL, Zhang YF, Dong PH, Zhang LX, Qin DH (2018) No post-drought compensatory growth of corns with root cutting based on cytokinin induced by roots. Agric Water Manag 205:9–20

    Article  Google Scholar 

  • Wang FH, Ahammed GJ, Li GY, Bai PT, Jiang Y, Wang SX, Chen SC (2019) Ethylene is involved in red light-induced anthocyanin biosynthesis in cabbage (Brassica oleracea). Int J Agric Biol 21:955–963

    CAS  Google Scholar 

  • Xu Z, Jiang Y, Zhou G (2015) Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front Plant Sci 6:701

    PubMed  PubMed Central  Google Scholar 

  • Yi CY, Yao KQ, Cai SY, Li HZ, Zhou J, Xia XJ, Shi K, Yu JQ, Foyer CH, Zhou YH (2015) High atmospheric carbon dioxide-dependent alleviation of salt stress is linked to RESPIRATORY BURST OXIDASE 1 (RBOH1)-dependent H2O2 production in tomato (Solanum lycopersicum). J Exp Bot 66(22):7391–7404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Yang Z, Jespersen D, Huang B (2014) Photosynthesis and protein metabolism associated with elevated CO2-mitigation of heat stress damages in tall fescue. Environ Exp Bot 99:75–85

    Article  CAS  Google Scholar 

  • Zhang S, Li X, Sun ZH, Shao SJ, Hu LF, Ye M, Zhou YH, Xia XJ, Yu JQ, Shi K (2015) Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. J Exp Bot 66(7):1951–1963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Pan CZ, Gu SH, Ma QM, Zhang YQ, Li X, Shi K (2018a) Stomatal movements are involved in elevated CO2-mitigated high temperature stress in tomato. Physiol Plant 165:569–583

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Hu ZJ, Lei C, Zheng CF, Wang J, Shao SJ, Li X, Xia XJ, Cai XZ, Zhou J, Zhou YH, Yu JQ, Foyer CH, Shi K (2018b) Plant phytosulfokine peptide initiates auxin-dependent immunity through cytosolic Ca2+ signaling in tomato. Plant Cell 30:652–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Xu XC, Cao JJ, Yin LL, Xia XJ, Shi K, Zhou YH, Yu JQ (2018) Heat shock factor HsfA1a is essential for R gene-mediated nematode resistance and triggers H2O2 production. Plant Physiol 176(3):2456–2471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zinta G, AbdElgawad H, Domagalska MA, Vergauwen L, Knapen D, Nijs I, Janssens IA, Beemster GT, Asard H (2014) Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels. Glob Change Biol 20(12):3670–3685

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2018YFD1000800), the Natural Science Foundation of Zhejiang Province for Distinguished Young Scholar (LR19C150001), the National Natural Science Foundation of China (31822046 and 31772355), and the Fundamental Research Funds for the Central Universities. We are grateful to the Tomato Genetics Resource Center at the University of California Davis, for kind advice on the Solanum lycopersicum L. cv. Ailsa Craig.

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Correspondence to Kai Shi.

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Pan, C., Zhang, H., Ma, Q. et al. Role of ethylene biosynthesis and signaling in elevated CO2-induced heat stress response in tomato. Planta 250, 563–572 (2019). https://doi.org/10.1007/s00425-019-03192-5

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