Differential physiological, transcriptomic and metabolomic responses of Arabidopsis leaves under prolonged warming and heat shock

Springer Science and Business Media LLC - Tập 20 - Trang 1-15 - 2020
Li Wang1,2, Kai-Biao Ma1, Zhao-Geng Lu1, Shi-Xiong Ren1, Hui-Ru Jiang1, Jia-Wen Cui1, Gang Chen3, Nian-Jun Teng4, Hon-Ming Lam2, Biao Jin1
1College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, China
2Center for Soybean Research of the State Key Laboratory of Agrobiotechnology and School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, China
3College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, China
4College of Horticulture, Nanjing Agricultural University, Nanjing, China

Tóm tắt

Elevated temperature as a result of global climate warming, either in form of sudden heatwave (heat shock) or prolonged warming, has profound effects on the growth and development of plants. However, how plants differentially respond to these two forms of elevated temperatures is largely unknown. Here we have therefore performed a comprehensive comparison of multi-level responses of Arabidopsis leaves to heat shock and prolonged warming. The plant responded to prolonged warming through decreased stomatal conductance, and to heat shock by increased transpiration. In carbon metabolism, the glycolysis pathway was enhanced while the tricarboxylic acid (TCA) cycle was inhibited under prolonged warming, and heat shock significantly limited the conversion of pyruvate into acetyl coenzyme A. The cellular concentration of hydrogen peroxide (H2O2) and the activities of antioxidant enzymes were increased under both conditions but exhibited a higher induction under heat shock. Interestingly, the transcription factors, class A1 heat shock factors (HSFA1s) and dehydration responsive element-binding proteins (DREBs), were up-regulated under heat shock, whereas with prolonged warming, other abiotic stress response pathways, especially basic leucine zipper factors (bZIPs) were up-regulated instead. Our findings reveal that Arabidopsis exhibits different response patterns under heat shock versus prolonged warming, and plants employ distinctly different response strategies to combat these two types of thermal stress.

Tài liệu tham khảo

Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: an overview. Environ Exp Bot. 2007;61:199–223. https://doi.org/10.1016/j.envexpbot.2007.05.011. Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, et al. Warming experiments underpredict plant phenological responses to climate change. Nature. 2012;485:494–7. https://doi.org/10.1038/nature11014. Springate DA, Kover PX. Plant responses to elevated temperatures: a field study on phenological sensitivity and fitness responses to simulated climate warming. Glob Chang Biol. 2014;20:456–65. https://doi.org/10.1111/gcb.12430. Hedhly A, Hormaza JI, Herrero M. Global warming and sexual plant reproduction. Trends Plant Sci. 2009;14:30–6. https://doi.org/10.1016/j.tplants.2008.11.001. Ainsworth EA, Ort DR. How do we improve crop production in a warming world? Plant Physiol. 2010;154:526–30. https://doi.org/10.1104/pp.110.161349. Lin D, Xia J, Wan S. Climate warming and biomass accumulation of terrestrial plants: a meta-analysis. New Phytol. 2010;188:187–98. https://doi.org/10.1111/j.1469-8137.2010.03347.x. Walther GR. Community and ecosystem responses to recent climate change. Philos T R Soc B. 2010;365:2019–24. https://doi.org/10.1098/rstb.2010.0021. Jin B, Li W, Jing W, Jiang KZ, Yang W, Jiang XX, Ni CY, Wang YL, Teng NJ. The effect of experimental warming on leaf functional traits, leaf structure and leaf biochemistry in Arabidopsis thaliana. BMC Plant Biol. 2011;11:35. https://doi.org/10.1186/1471-2229-11-35. Way DA, Yamori W. Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynth Res. 2014;119:89–100. https://doi.org/10.1007/s11120-013-9873-7. Glaubitz U, Li X, Schaedel S, Erban A, Sulpice R, Kopka J, Hincha DK, Zuther E. Integrated analysis of rice transcriptomic and metabolomic responses to elevated night temperatures identifies sensitivity- and tolerance-related profiles. Plant Cell Environ. 2017;40:121–37. https://doi.org/10.1111/pce.12850. Pospíšil P. Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Front Plant Sci. 2016;7:1950. https://doi.org/10.3389/fpls.2016.01950. Bita CE, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4:273. https://doi.org/10.3389/fpls.2013.00273. Ohama N, Sato H, Shinozaki K, Yamaguchishinozaki K. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 2017;22:53–65. https://doi.org/10.1016/j.tplants.2016.08.015. Niu Y, Xiang Y. An overview of biomembrane functions in plant responses to high-temperature stress. Front Plant Sci. 2018;9:915. https://doi.org/10.3389/fpls.2018.00915. Atkin OK, Loveys BR, Atkinson LJ, Pons TL. Phenotypic plasticity and growth temperature: understanding interspecific variability. J Exp Bot. 2006;57:267–81. https://doi.org/10.1093/jxb/erj029. Ashraf M, Harris PJC. Photosynthesis under stressful environments: an overview. Photosynthetica. 2013;51:163–90. https://doi.org/10.1007/s11099-013-0021-6. Sakata S, Mizusawa N, Kubotakawai H, Sakurai I, Wada H. Psb28 is involved in recovery of photosystem II at high temperature in Synechocystis sp. PCC 6803. Biochim Biophys Acta. 2013;1827:50–9. https://doi.org/10.1016/j.bbabio.2012.10.004. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res. 2008;98:541–50. https://doi.org/10.1007/s11120-008-9331-0. Patrick JW, Botha FC, Birch RG. Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnol J. 2013;11:142–56. https://doi.org/10.1111/pbi.12002. Dumschott K, Richter A, Loescher W, Merchant A. Post photosynthetic carbon partitioning to sugar alcohols and consequences for plant growth. Phytochemistry. 2017;144:243–52. https://doi.org/10.1016/j.phytochem.2017.09.019. Lismont C, Nordgren M, Van Veldhoven PP, Fransen M. Redox interplay between mitochondria and peroxisomes. Front Cell Dev Biol. 2015;3:35. https://doi.org/10.3389/fcell.2015.00035. Dietz KJ, Turkan I, Krieger-Liszkay A. Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol. 2016;171:1541–50. https://doi.org/10.1104/pp.16.00375. Sun AZ, Guo FQ. Chloroplast retrograde regulation of heat stress responses in plants. Front Plant Sci. 2016;7:398. https://doi.org/10.3389/fpls.2016.00398. Grover A, Mittal D, Negi M, Lavania D. Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci. 2013;205-206:38–47. https://doi.org/10.1016/j.plantsci.2013.01.005. Zhao J, He Q, Chen G, Wang L, Jin B. Regulation of non-coding RNAs in heat stress responses of plants. Front Plant Sci. 2016;7:1213. https://doi.org/10.3389/fpls.2016.01213. Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, et al. Arabidopsis HSFA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Gen Genomics. 2011;286:321–32. https://doi.org/10.1007/s00438-011-0647-7. Srivastava R, Deng Y, Howell SH. Stress sensing in plants by an ER stress sensor/transducer, bZIP28. Front Plant Sci. 2014;5:59. https://doi.org/10.3389/fpls.2014.00059. Bäurle I. Plant heat adaptation: priming in response to heat stress. F1000research. 2016;5:694. https://doi.org/10.12688/f1000research.7526.1. Lämke J, Brzezinka K, Altmann S, Bäurle I. A hit- and -run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. 2016;35:162–75. https://doi.org/10.15252/embj.201592593. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2006;2:e106. https://doi.org/10.1371/journal.pgen.0020106. Flato G, Marotzke J, Abiodun B, Braconnot P, Chou SC, Collins WJ, et al. Evaluation of climate models. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, editors. Climate Change. 2013: The physical science basis. contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change, vol. 5. Cambridge: Cambridge University Press; 2013. p. 741–866. Boyes DC, Zayed AM, Ascenzi R, Mccaskill AJ, Hoffman NE, Davis KR, Görlach J. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell. 2001;13:1499–510. https://doi.org/10.1105/tpc.13.7.1499. Ren S, Ma K, Lu Z, Chen G, Cui J, Tong P, Wang L, Teng N, Jin B. Transcriptomic and metabolomic analysis of the heat-stress response of Populus tomentosa Carr. Forests. 2019;10:383. https://doi.org/10.3390/f10050383. Allen P, Bennett K, King J. PASW statistics by SPSS, a practical guide: version 18.0. Melbourne: Cengage Learning Press; 2010.