Photoprotective and antioxidative mechanisms against oxidative damage in Fargesia rufa subjected to drought and salinity
Cheng-Gang Liu A E , Qing-Wei Wang B , Yan-Qiang Jin C , Kai-Wen Pan C and Yan-Jie Wang C D E
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, 666 303, China.
B Graduate School of Life Sciences, Tohoku University, Aoba, Sendai, 980-8578, Japan.
C Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610 041, China.
D College of Life Science, Sichuan Normal University, Chengdu, 610 101, China.
E Corresponding authors. Emails: chenggangliu@hotmail.com; wyjilwm2015@163.com
Functional Plant Biology 44(3) 302-311 https://doi.org/10.1071/FP16214
Submitted: 13 June 2016 Accepted: 8 November 2016 Published: 5 January 2017
Abstract
Drought and salinity are the two most common and frequently co-occurring abiotic stresses limiting plant productivity worldwide, yet it remains unclear whether bamboo species possess effective mechanisms to protect against oxidative damage caused by drought and salinity, either alone or in combination. In this study, we utilised Fargesia rufa Yi, a species important to forest carbon sequestration and endangered giant pandas, to evaluate physiological, biochemical and ultrastructural responses to drought, salinity and their combination. Under drought alone, F. rufa exhibited reduced water loss from leaves, photochemistry inhibition, pigment degradation, reactive oxygen species accumulation, lipid peroxidation, and damage to organelles compared with salinity and combined stress treatments. The superior performance under drought alone was attributed to greater thermal dissipation and the water-water cycle capacities, increased SOD/AsA-GSH cycle enzymes activities, and a favourable redox balance of antioxidants. Therefore, relative to salinity alone and drought + salinity, F. rufa plants under drought exhibit highly efficient mechanisms to protect against oxidative damage, which most likely allow accelerated recovery of photosynthetic plasticity once the stress is removed.
Additional keywords: antioxidative enzymes, bamboo, drought, electron transport, leaf ultrastructure, salt stress.
References
Abogadallah GM (2011) Differential regulation of photorespiratory gene expression by moderate and severe salt and drought stress in relation to oxidative stress. Plant Science 180, 540–547.| Differential regulation of photorespiratory gene expression by moderate and severe salt and drought stress in relation to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFShug%3D%3D&md5=783b3a3a3ca835b08eb5b68d8e69c27bCAS |
Ahmed IM, Nadira UA, Bibi N, Cao FB, He XY, Zhang GP, Wu FB (2015) Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environmental and Experimental Botany 111, 1–12.
| Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVGit7jN&md5=196e3656ca8cdf884c24ce5bc2a33a5cCAS |
Arrigoni O, Dipierro S, Borraccino G (1981) Ascorbate free radical reductase, a key enzyme of the ascorbic acid system. FEBS Letters 125, 242–244.
| Ascorbate free radical reductase, a key enzyme of the ascorbic acid system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhsFalsLs%3D&md5=ced64589070f728cef8741ac399cb5e0CAS |
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiology 98, 1222–1227.
| Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVCgsro%3D&md5=08d617b11061e7d287d3d13578a81817CAS |
Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. Journal of Experimental Botany 55, 2365–2384.
| Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVOisr0%3D&md5=25d7be66d65cdf83f1c00891742b349fCAS |
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
| Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7s%3D&md5=e68ffae239ea6d79d2c239824f21a16eCAS |
Chen LH, Zhang S, Zhao HX, Korpelainen H, Li CY (2010) Sex-related adaptive responses to interaction of drought and salinity in Populus yunnanensis. Plant, Cell & Environment 33, 1767–1778.
| Sex-related adaptive responses to interaction of drought and salinity in Populus yunnanensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlemsbfI&md5=cb7f9d6d5309e958db08408ce1ff7d22CAS |
Chen JW, Kuang SB, Long GQ, Yang SC, Meng ZG, Li LG, Chen ZJ, Zhang GH (2016) Photosynthesis, light energy partitioning, and photoprotection in the shade-demanding species Panax notoginseng under high and low level of growth irradiance. Functional Plant Biology 43, 479–491.
| Photosynthesis, light energy partitioning, and photoprotection in the shade-demanding species Panax notoginseng under high and low level of growth irradiance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XosFaqsro%3D&md5=f2ecc4778414452d0b90a7c1c512d5f7CAS |
Dawalibi V, Monteverdi MC, Moscatello S, Battistelli A, Valentini R (2015) Effect of salt and drought on growth, physiological and biochemical responses of two Tamarix species. iForest-Biogeosciences and Forestry 8, 772–779.
| Effect of salt and drought on growth, physiological and biochemical responses of two Tamarix species.Crossref | GoogleScholarGoogle Scholar |
Driever SM, Baker NR (2011) The water-water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted. Plant, Cell & Environment 34, 837–846.
| The water-water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVGksL0%3D&md5=754cab277c3b01b2b8fb3aff8a0febd1CAS |
Filippou P, Bouchagier P, Skotti E, Fotopoulos V (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environmental and Experimental Botany 97, 1–10.
| Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGmu73N&md5=4e0af2f284b78675782efbb17e2cfdd2CAS |
Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343–352.
| Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhu7o%3D&md5=f33d3d5a29c9759f29ee6c21e6c322f7CAS |
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21–25.
| The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2czlsVeltA%3D%3D&md5=aa5e917cc8f2851aa0b02b36fcfdb226CAS |
Fusaro L, Mereu S, Brunetti C, Ferdinando MD, Ferrini F, Manes F, Salvatori E, Marzuoli R, Gerosa G, Tattini M (2014) Photosynthetic performance and biochemical adjustments in two co-occurring Mediterranean evergreens, Quercus ilex and Arbutus unedo, differing in salt-exclusion ability. Functional Plant Biology 41, 391–400.
| Photosynthetic performance and biochemical adjustments in two co-occurring Mediterranean evergreens, Quercus ilex and Arbutus unedo, differing in salt-exclusion ability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlCnu7Y%3D&md5=c788a6e62b2ef3180efc2c6ab56324aaCAS |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiology 59, 309–314.
| Superoxide dismutases. I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhtlKgtrs%3D&md5=6fb84ec18e9ef95b5943a146c9cbb149CAS |
Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynthesis Research 82, 73–81.
| A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlersr0%3D&md5=c3b4691ccdb903f21d0ad78f488a36f4CAS |
Hirotsu N, Makino A, Ushio A, Mae T (2004) Changes in the thermal dissipation and the electron flow in the water–water cycle in rice grown under conditions of physiologically low temperature. Plant & Cell Physiology 45, 635–644.
| Changes in the thermal dissipation and the electron flow in the water–water cycle in rice grown under conditions of physiologically low temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1Klu74%3D&md5=711a825513ca95e64850001ddce83bacCAS |
Li YP, Zhang YB, Zhang XL, Korpelainen H, Berninger F, Li CY (2013) Effects of elevated CO2 and temperature on photosynthesis and leaf traits of an understory dwarf bamboo in subalpine forest zone, China. Physiologia Plantarum 148, 261–272.
| Effects of elevated CO2 and temperature on photosynthesis and leaf traits of an understory dwarf bamboo in subalpine forest zone, China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptlOnsr4%3D&md5=cd2e6ff404c9d2fcfd4d841222240b9cCAS |
Liu CG, Wang YJ, Pan KW, Li W, Zhang L, Shen XY, Liu LJ, Deng MR (2014) Responses of the antioxidant defense system to drought stress in the leaves of Fargesia denudata seedlings, the staple food of the giant panda. Russian Journal of Plant Physiology 61, 374–383.
| Responses of the antioxidant defense system to drought stress in the leaves of Fargesia denudata seedlings, the staple food of the giant panda.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntFGjsr8%3D&md5=e52e1134bc9ea8441ccf2b51dcb3fb94CAS |
Liu CG, Wang YJ, Pan KW, Jin YQ, Li W, Zhang L (2015a) Effects of phosphorus application on photosynthetic carbon and nitrogen metabolism, water use efficiency and growth of dwarf bamboo (Fargesia rufa) subjected to water deficit. Plant Physiology and Biochemistry 96, 20–28.
| Effects of phosphorus application on photosynthetic carbon and nitrogen metabolism, water use efficiency and growth of dwarf bamboo (Fargesia rufa) subjected to water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Crsb%2FI&md5=0b938231a28752d8ac8186c8c85005f6CAS |
Liu CG, Wang YJ, Pan KW, Jin YQ, Liang J, Li W, Zhang L (2015b) Photosynthetic carbon and nitrogen metabolism and the relationship between their metabolites and lipid peroxidation in dwarf bamboo (Fargesia rufa Yi) during drought and subsequent recovery. Trees 29, 1633–1647.
| Photosynthetic carbon and nitrogen metabolism and the relationship between their metabolites and lipid peroxidation in dwarf bamboo (Fargesia rufa Yi) during drought and subsequent recovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFSjt7zJ&md5=c294a46c5e085f140ce9f231551740aaCAS |
Miyake C, Yokota A (2000) Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis. Plant & Cell Physiology 41, 335–343.
| Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFegtLY%3D&md5=cf8383bce64b4e4f09c63e539e6214b5CAS |
Morari F, Meggio F, Lunardon A, Scudiero E, Forestan C, Farinati S, Varotto S (2015) Time course of biochemical, physiological, and molecular responses to field-mimicked conditions of drought, salinity, and recovery in two maize lines. Frontiers in Plant Science 6, 314
| Time course of biochemical, physiological, and molecular responses to field-mimicked conditions of drought, salinity, and recovery in two maize lines.Crossref | GoogleScholarGoogle Scholar |
Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Non-photochemical quenching. A response to excess light energy.Crossref | GoogleScholarGoogle Scholar |
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
| Genes and salt tolerance: bringing them together.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGisbfP&md5=46becc7a1e424d003d4069d156fe8544CAS |
Muscolo A, Junker A, Klukas C, Weigelt-Fischer K, Riewe D, Altmann T (2015) Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. Journal of Experimental Botany 66, 5467–5480.
| Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVKnt77F&md5=2fc6bb5514a53ddf29a19e98404644c1CAS |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Razzaghi F, Jacobsen SE, Jensen CR, Andersen MN (2015) Ionic and photosynthetic homeostasis in quinoa challenged by salinity and drought-mechanisms of tolerance. Functional Plant Biology 42, 136–148.
| Ionic and photosynthetic homeostasis in quinoa challenged by salinity and drought-mechanisms of tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsFChsw%3D%3D&md5=76085c54cc8221c91d4f0a05050a07bfCAS |
Scurlock JMO, Dayton DC, Hames B (2000) Bamboo: an overlooked biomass resource? Biomass and Bioenergy 19, 229–244.
| Bamboo: an overlooked biomass resource?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVCntbk%3D&md5=c4aa701bc1ac9f9b5be93b5df1c21bbbCAS |
Silva EN, Ferreira-Silva SL, Fontenele Ad V, Ribeiro RV, Viégas RA, Silveira JAG (2010) Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants. Journal of Plant Physiology 167, 1157–1164.
| Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsVCls7g%3D&md5=d0a55877875e2d7cb79e75321f0f7b81CAS |
Silva EN, Silveira JA, Ribeiro RV, Vieira SA (2015) Photoprotective function of energy dissipation by thermal processes and photorespiratory mechanisms in Jatropha curcas plants during different intensities of drought and after recovery. Environmental and Experimental Botany 110, 36–45.
| Photoprotective function of energy dissipation by thermal processes and photorespiratory mechanisms in Jatropha curcas plants during different intensities of drought and after recovery.Crossref | GoogleScholarGoogle Scholar |
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytologist 203, 32–43.
| Abiotic and biotic stress combinations.Crossref | GoogleScholarGoogle Scholar |
Szalai G, Kellős T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. Journal of Plant Growth Regulation 28, 66–80.
| Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvF2qt74%3D&md5=856e5bda50b60e4fe05e98bf0b56fbd9CAS |
Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.
| Leaf xanthophyll content and composition in sun and shade determined by HPLC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslGrtr4%3D&md5=3304b39688edcc7ebdefca21b9d24e62CAS |
Tuanmu MN, Viña A, Winkler JA, Li Y, Xu WH, Ouyang ZY, Liu JG (2013) Climate-change impacts on understorey bamboo species and giant pandas in China’s Qinling Mountains. Nature Climate Change 3, 249–253.
| Climate-change impacts on understorey bamboo species and giant pandas in China’s Qinling Mountains.Crossref | GoogleScholarGoogle Scholar |
Yen TM, Ji YJ, Lee JS (2010) Estimating biomass production and carbon storage for a fast-growing makino bamboo (Phyllostachys makinoi) plant based on the diameter distribution model. Forest Ecology and Management 260, 339–344.
| Estimating biomass production and carbon storage for a fast-growing makino bamboo (Phyllostachys makinoi) plant based on the diameter distribution model.Crossref | GoogleScholarGoogle Scholar |
Yi XP, Zhang YL, Yao HS, Luo HH, Gou L, Chow WS, Zhang WF (2016) Different strategies of acclimation of photosynthesis, electron transport and antioxidative activity in leaves of two cotton species to water deficit. Functional Plant Biology 43, 448–460.
Yuan YH, Shu S, Li SH, He LZ, Li H, Du NS, Sun J, Guo SR (2014) Effects of exogenous putrescine on chlorophyll fluorescence imaging and heat dissipation capacity in cucumber (Cucumis sativus L.) under salt stress. Journal of Plant Growth Regulation 33, 798–808.
| Effects of exogenous putrescine on chlorophyll fluorescence imaging and heat dissipation capacity in cucumber (Cucumis sativus L.) under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXos1akur8%3D&md5=4b9ede4a3b82ad47ac176209e8ad5a61CAS |
Zhang Q, Zhang TJ, Chow WS, Xie X, Chen YJ, Peng CL (2015) Photosynthetic characteristics and light energy conversions under different light environments in five tree species occupying dominant status at different stages of subtropical forest succession. Functional Plant Biology 42, 609–619.
| Photosynthetic characteristics and light energy conversions under different light environments in five tree species occupying dominant status at different stages of subtropical forest succession.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXps1Okurc%3D&md5=416d13ab246399417fa29b30f184a6caCAS |
