5-羟色胺在红树植物秋茄幼苗抗寒中的作用

doi:10.13287/j.1001-9332.202305.013

摘要/Abstract

摘要： 5-羟色胺(5-HT)不仅能参与植物的生长发育,还可以延缓衰老及应对非生物胁迫。为探明5-HT在调控红树林抗寒中的作用,以红树植物秋茄为试验材料,研究抗寒锻炼和喷施DL-4-氯苯丙氨酸(p-CPA, 5-HT合成抑制剂)对低温胁迫下秋茄幼苗叶片气体交换参数、CO₂响应曲线(A/Ca)和内源植物激素含量的影响。结果表明: 低温胁迫显著降低了秋茄幼苗叶片5-HT、叶绿素、内源生长素(IAA)、赤霉素(GA)和脱落酸(ABA)含量,减弱了其利用CO₂的能力,降低了净光合速率,抑制了初始羧化效率。低温胁迫下施用外源p-CPA降低了秋茄幼苗叶片光合色素、内源各激素和5-HT含量,加剧了低温胁迫对秋茄幼苗叶片光合功能的伤害。抗寒锻炼可有效降低低温胁迫下秋茄幼苗叶片内源IAA含量,促使植株产生更多的5-HT,提高了叶片光合色素、GA、ABA含量和初始羧化效率,提升了光合碳同化能力,最终提高了秋茄幼苗叶片的光合作用;抗寒锻炼下喷施p-CPA会显著抑制秋茄幼苗叶片5-HT合成,促进IAA产生,同时降低光合色素、GA、ABA含量和初始羧化效率,减弱抗寒锻炼对红树林抗寒性的提高作用。综上所述,抗寒锻炼通过调控光合碳同化能力和内源植物激素含量提高秋茄幼苗的抗寒性,5-HT的合成是提高红树林抗寒性的必要条件之一。

关键词: 抗寒锻炼, 低温胁迫, 红树林, CO₂响应曲线, 光合作用, 5-羟色胺, 内源激素

Abstract: 5-hydroxytryptamine (5-HT) participates in plant growth and development, and can also delay senescence and cope with abiotic stress. To explore the role of 5-HT in regulating the abilities of mangrove in cold resis-tance, we examined the effects of cold acclimation and the spraying of p-chlorophenylalanine (p-CPA, 5-HT synthesis inhibitor) on leaf gas exchange parameters and CO₂ response curves (A/Ca), as well as the endogenous phytohormone content levels in the mangrove species Kandelia obovata seedlings under low temperature stress. The results showed that low temperature stress significantly reduced the contents of 5-HT, chlorophyll, endogenous auxin (IAA), gibberellin (GA), and abscisic acid (ABA). It weakened the CO₂ utilization abilities of plants and reduced net photosynthetic rate, which ultimately reduced carboxylation efficiency (CE). Under low temperature stress, exogenous p-CPA reduced the contents of photosynthetic pigments, endogenous hormones, and 5-HT in the leaves, which aggravated the damages caused by low temperature stress on photosynthesis. By enhancing cold acclimation abilities, the endogenous IAA content in the leaves could was reduced under low temperature stress, promoted the production of 5-HT, improved the contents of photosynthetic pigments, GA, and ABA, as well as enhanced photosynthetic carbon assimilation abilities, which would increase photosynthesis in the K. obovata seedlings. Under cold acclimation conditions, the spraying of p-CPA could significantly inhibit the synthesis of 5-HT, promote the production of IAA, and reduce the contents of photosynthetic pigments, GA, ABA, and CE, which would weaken the effects of cold acclimation by improving the cold resistance of mangroves. In conclusion, cold acclimation could improve the cold resistance abilities of K. obovata seedlings by regulating photosynthetic carbon assimilation capacity and the contents of endogenous phytohormone. 5-HT synthesis is one of the necessary conditions for improving the cold resistance abilities of mangroves.

Key words: cold acclimation, low temperature stress, mangrove, CO₂ response curve, photosynthesis, 5-HT, endogenous phytohormone

张慧玉, 岳丹斐, 潘晓娇, 郝露露, 刘伟成, 郑春芳. 5-羟色胺在红树植物秋茄幼苗抗寒中的作用[J]. 应用生态学报, 2023, 34(5): 1263-1271.

ZHANG Huiyu, YUE Danfei, PAN Xiaojiao, HAO Lulu, LIU Weicheng, ZHENG Chunfang. Effects of 5-HT on the cold resistance of mangrove Kandelia obovata seedlings[J]. Chinese Journal of Applied Ecology, 2023, 34(5): 1263-1271.

参考文献

[1] Quisthoudt K, Schmitz N, Randin CF, et al. Temperature variation among mangrove latitudinal range limits worldwide. Trees, 2012, 26: 1919-1931
[2] Cohen MC, Souza AV, Liu K, et al. Effects of the 2017-2018 winter freeze on the northern limit of the American mangroves, Mississippi River delta plain. Gemorpho-logy, 2021, 394: 107968
[3] Zheng CF, Ye Y, Liu WC, et al. Recovery of photosynthesis, sucrose metabolism, and proteolytic enzymes in Kandelia obovata from rare cold events in the northernmost mangrove, China. Ecological Processes, 2016, 5: 9
[4] Juurakko CL, DiCenzo GC, Walker VK. Cold acclimation and prospects for cold-resilient crops. Plant Stress, 2021, 2: 100028
[5] 赵金梅, 阿拉木斯, 梁燕, 等. 抗寒锻炼对紫花苜蓿抗寒性和生长特性的影响. 中国草地学报, 2020, 41(6): 30-36
[6] Xu K, Zhao Y, Gu J, et al. Proteomic analysis reveals the molecular mechanism underlying the cold acclimation and freezing tolerance of wheat (Triticum aestivum L.). Plant Science, 2022, 318: 111242
[7] Přerostová S, Zupková B, Petřík I, et al. Hormonal responses associated with acclimation to freezing stress in Lolium perenne. Environmental and Experimental Botany, 2021, 182: 104295
[8] Liang G, Ma Z, Lu S, et al. Temperature-phase transcriptomics reveals that hormones and sugars in the phloem of grape participate in tolerance during cold acclimation. Plant Cell Reports, 2022, 41: 1357-1373
[9] Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, et al. Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant and Cell Physiology, 2011, 52: 490-508
[10] Erland LA, Turi CE, Saxena PK. Serotonin: An ancient molecule and an important regulator of plant processes. Biotechnology Advances, 2016, 34: 1347-1361
[11] Liu Y, Ding XY, Lv Y, et al. Exogenous serotonin improves salt tolerance in rapeseed (Brassica napus L.) seedlings. Agronomy, 2021, 11: 400
[12] 田姗姗, 李继强, 邹锡玲, 等. 5-羟色胺对油菜幼苗干旱的缓解效应. 中国油料作物学报, 2019, 41(2): 192-198
[13] 黄贺. 5-羟色胺与褪黑素提高油菜低温耐性的效应研究. 硕士论文. 北京: 中国农业科学院, 2020
[14] Shen Z, Qin Y, Luo M, et al. Proteome analysis reveals a systematic response of cold-acclimated seedlings of an exotic mangrove plant Sonneratia apetala to chilling stress. Journal of Proteomics, 2021, 248: 104349
[15] Deryabina IB, Andrianov VV, Muranova LN, et al. Effects of thryptophan hydroxylase blockade by P-Chlorophenylalanine on contextual memory reconsolidation after training of different intensity. International Journal of Molecular Sciences, 2020, 21: 2087
[16] Ramakrishna A, Giridhar P, Ravishankar GA. Indo-leamines and calcium channels influence morphogenesis in in vitro cultures of Mimosa pudica L. Plant Signaling & Behavior, 2009, 4: 1136-1141
[17] Wang X, Cai J, Jiang D, et al. Pre-anthesis high-tempe-rature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. Journal of Plant Physiology, 2011, 168: 585-593
[18] 叶子飘, 高峻. 丹参羧化效率在其CO₂补偿点附近的变化. 西北农林科技大学学报: 自然科学版, 2008, 36(5): 160-164
[19] Tal O, Haim A, Harel O, et al. Melatonin as an antio-xidant and its semi-lunar rhythm in green macroalga Ulva sp. Journal of Experimental Botany, 2011, 62: 1903-1910
[20] Liu WC, Zheng CF, Chen JN, et al. Cold acclimation improves photosynthesis by regulating the ascorbate-glutathione cycle in chloroplasts of Kandelia obovate. Journal of Forestry Research, 2019, 30: 755-765
[21] Ding F, Ren L, Xie F, et al. Jasmonate and melatonin act synergistically to potentiate cold tolerance in tomato plants. Frontiers in Plant Science, 2021, 12: 763284
[22] 罗辅燕, 陈卫英, 陈真勇. 指数改进模型在大麦光合-CO₂响应曲线中的适用性. 植物生态学报, 2013, 37(7): 650-655
[23] Coste S, Roggy JC, Imbert P, et al. Leaf photosynthetic traits of 14 tropical rain forest species in relation to leaf nitrogen concentration and shade tolerance. Tree Physio-logy, 2005, 25: 1127-1137
[24] Dahal K, Knowles VL, Plaxton WC, et al. Enhancement of photosynthetic performance, water use efficiency and grain yield during long-term growth under elevated CO₂ in wheat and rye is growth temperature and cultivar dependent. Environmental and Experimental Botany, 2014, 106: 207-220
[25] Pociecha E, Dziurka M, Waligórski P, et al. Brassinosteroids increase winter survival of winter rye (Secale cereale L.) by affecting photosynthetic capacity and carbohydrate metabolism during the cold acclimation process. Plant Growth Regulation, 2016, 80: 127-135
[26] Pociecha E, Dziurka M, Waligórski P, et al. 24-Epibrassinolide pre-treatment modifies cold-induced photosynthetic acclimation mechanisms and phytohormone response of perennial ryegrass in cultivar-dependent manner. Journal of Plant Growth Regulation, 2017, 36: 618-628
[27] Lu T, Song Y, Yu H, et al. Cold stress resistance of tomato (Solanum lycopersicum) seedlings is enhanced by light supplementation from underneath the canopy. Frontiers in Plant Science, 2022, 13: 831314
[28] Dharmawardhana P, Ren L, Amarasinghe V, et al. A genome scale metabolic network for rice and accompanying analysis of tryptophan, auxin and serotonin biosynthesis regulation under biotic stress. Rice, 2013, 6: 15
[29] Mukherjee S, David A, Yadav S, et al. Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflo-wer seedling roots and cotyledons. Physiologia Plantarum, 2014, 152: 714-728
[30] 卞凤娥, 唐翠花, 邢浩, 等. 外源褪黑素对干旱胁迫下葡萄内源褪黑素及叶绿素荧光特性的影响. 植物生理学报, 2018, 54(10): 1615-1623
[31] Guo B, Stiles AR, Liu CZ. Changes in endogenous hormones and oxidative burst as the biochemical basis for enhanced shoot organogenesis in cold-treated Saussurea involucrata explants. Acta Physiologiae Plantarum, 2012, 35: 283-287
[32] Olien CR, Smith MN. Analysis and Improvement of Plant Cold Hardiness. Boca Raton, FL, USA: CRC Press, 1981
[33] 王成. 非生物逆境胁迫下5-羟色胺合成的调控研究. 硕士论文. 武汉: 华中农业大学, 2014
[34] Cai S, Jiang G, Ye N, et al. A key ABA catabolic gene, OsABA8ox3, is involved in drought stress resis-tance in rice. PLoS One, 2015, 10(2): e0116646
[35] Soitamo AJ, Piippo M, Allahverdiyeva Y, et al. Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biology, 2008, 8: 13
[36] Lang V, Mantyla E, Welin B, et al. Alterations in water status, endogenous abscisic acid content, and expression of Rab18 gene during the development of freezing tole-rance in Arabidopsis thaliana. Plant Physiology, 1994, 104: 1341-1349
[37] 冯玲. 脱落酸介导5-羟色胺调控水稻对褐飞虱的抗性研究. 硕士论文. 江苏扬州: 扬州大学, 2022
[38] 田小霞, 孟林, 毛培春, 等. 低温条件下不同抗寒性薰衣草内源激素的变化. 植物生理学报, 2014, 50(11): 1669-1674
[39] 刘学庆, 孙纪霞, 丁朋松, 等. 低温胁迫对蝴蝶兰内源激素的影响. 江西农业大学学报, 2012, 34(3): 464-469
[40] 罗正荣. 植物激素与抗寒力的关系. 植物生理学通讯, 1989(3): 1-5