Responses of Heat Dissipation in Rice to Stress

doi:10.16819/j.1001-7216.2016.6003

Abstract

Abstract:

Nonphotochemistry quenching (NPQ) has been used to estimate the level of heat dissipation,which is originally transformed from light energy. Heat dissipation plays a key role in maintaining the balance of light energy transformation, and it is the main mechanism of rice leaf to deal with excessive light energy. Numbers of previous studies have demonstrated that the induced process of heat dissipation is regulated by ΔpH across thylakoid membrane, xanthophyll cycle and PsbS protein, etc. The relationship between NPQ and photoprotection is not linear.NPQ only acts as an effective indicator of photoprotection in some specified situation. Heat dissipation is closely related with the stress resistance of rice in that NPQ level in rice leaf increases under stress conditions of heat, chilling, nitrogen deficiency and drought. This paper reviews the recent progress of heat dissipation, and mainly by summarizing the induction and regulation procedure of heat dissipation, the relationship of NPQ and photoprotection and the response of NPQ to environmental factors, such as temperature, nitrogen nutrition,water and salt. The research prospects on the relationship of NPQ and photoprotection of rice is also discussed.

Key words: rice, heat dissipation, photosynthesis, photoprotection, stress

摘要：

非光化学猝灭（NPQ）常用于评估以热能途径耗散的光能（热耗散），热耗散在维持光能转化平衡中起着重要作用，是水稻叶片重要的光防御机制。大量研究表明，热耗散的诱导受跨类囊体膜ΔpH、叶黄素循环和PsbS蛋白等的调控；NPQ与光保护效应不呈线性关系，只有在某些特定条件下，NPQ才可作为光保护效应的有效指标；在高温、低温、缺氮、干旱、盐胁迫等逆境下水稻NPQ显著增加，热耗散可能与水稻抗逆性密切相关。本文从热耗散的诱导和调控机制、NPQ与光保护效应以及水稻NPQ对环境因子（温度、氮营养、水分、盐）的响应等4个方面综述了水稻叶片热耗散的研究进展，并对水稻NPQ与抗逆性关系的研究作了展望。

关键词: 水稻, 热耗散, 光合作用, 光保护, 逆境

CLC Number:

ZHAO Xia1,2,#,YANG Huawei1,#,LIU Ranfang1, CHEN Tingting2, FENG Baohua2, ZHANG Caixia2, YANG Xueqin2, TAO Longxing2,* . Responses of Heat Dissipation in Rice to Stress[J]. Chinese Journal of Rice Science, DOI: 10.16819/j.1001-7216.2016.6003 .

赵霞1,2,#,杨华伟1,#,刘然方1,陈婷婷2,奉保华2,张彩霞2,杨雪芹2,陶龙兴2,*. 水稻热耗散对逆境的响应[J]. 中国水稻科学, DOI: 10.16819/j.1001-7216.2016.6003 .

References

[1]Baker N R． Chlorophyll fluorescence： A probe of photosynthesis in vivo． Annu Rev Plant Biol, 2008，59：89113．
[2]Ji B， Jiao D． Photoinhibition and photooxidation in leaves of indica and japonica rice under different temperatures and light intensities．Acta Bot Sin, 2000，43（7）：714720．
[3]Maxwell K, Johnson G N．Chlorophyll fluorescence-a practical guide．J Exp Bot, 2000, 51（345）：659668．
[4]Duysens L, Sweers H. Mechanism of two photochemical reactions in algae as studied by means of fluorescence. Stud Microal Photosyn Bac, 1963：353372.
[5]Papageorgiou G. Lightinduced changes in the fluorescence yield of chlorophyllain vivo：Ⅰ. Anacystis nidulans. Biophys J, 1968, 8（11）：12991315.
[6]Wraight C A, Crofts A R. Energy dependent quenching of chlorophyll a fluorescence in isolated chloroplasts. Eur J Biochem, 1970, 17（2）：319327.
[7]Johnson G, Young A, Scholes J, et al. The dissipation of excess excitation energy in British plant species. Plant, Cell Environ, 1993, 16（6）：673679.
[8]Horton P. Developments in research on nonphotochemical fluorescence quenching：Emergence of key ideas, theories and experimental approaches. NonPhotochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Dordrecht, Springer, 2014：7395.
[9]Zhu X G, Ort D R, Whitmarsh J, et al. The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies：A theoretical analysis. J Exp Bot, 2004, 55（400）：11671175.
[10]Li Y, Ren B, Gao L, et al. Less chlorophyll does not necessarily restrain light capture ability and photosynthesis in a chlorophylldeficient rice mutant. J Agron Crop Sci, 2013, 199： 4956.
[11]欧立军. 水稻叶色突变体的高光合特性. 作物学报, 2011, 37（10）：18601867.
Ou L J. High photosynthetic efficiency of leaf colour mutant of rice (Oryza sativa L.). Acta Bot Sin, 2011, 37（10）：18601867（in Chinese with English abstract）.
[12]Wang Q, Zhang Q D, Zhu X G, et al. PS Ⅱ photochemistry and xanthophyll cycle in two superhighyield rice hybrids, Liangyoupeijiu and Huaan 3 during photoinhibition and subsequent restoration. Acta Bot Sin, 2002, 44（11）：12971302.
[13]Lazár D. Parameters of photosynthetic energy partitioning. J Plant Physiol, 2015, 175：131147.
[14]Goss R, Lepetit B. Biodiversity of NPQ. J Plant Physiol, 2015, 172（1）：1332.
[15]Morales F, Abadía J, Abadía A. Thermal energy dissipation in plants under unfavorable soil conditions. NonPhotochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Dordrecht, Springer, 2014：605630.
[16]DemmigAdams B, Stewart J J, Adams W W. Chloroplast Photoprotection and the TradeOff Between Abiotic and Biotic Defense. NonPhotochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Dordrecht, Springer, 2014：631643.
[17]王强. 超高产杂交稻（Oryza sativa L）光合作用和光抑制的研究. 北京：中国科学院， 2002.
Wang Q. Photosynthesis and photoinhibition of two superhighyield rice hybrids, Liangyoupeijiu and Huaan 3. Beijing：Chinese Academy of Sciences, 2002. （in Chinese with English abstract）.
[18]Kasajima I, Ebana K, Yamamoto T, et al. Molecular distinction in genetic regulation of nonphotochemical quenching in rice. PNAS, 2011, 108（33）：1383513840.
[19]Foyer CH, Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol, 2011, 155（1）：93100.
[20]赵明, 姜雯, 丁在松, 等. 玉米和小麦在光合诱导期间非光化学猝灭（qN）差异. 作物学报, 2006, 31（12）：15441551.
Zhao M, Jiang W, ding Z S, et al. Differences between maize and wheat for nonphotochemical quenching (qN)during photosynthetic induction. Acta Bot Sin, 2006, 31（12）：15441551. （in Chinese with English abstract）.
[21]Ikeuchi M, Uebayashi N, Sato F, et al. Physiological functions of PsbSdependent and PsbSindependent NPQ under naturally fluctuating light conditions. Plant Cell Physiol, 2014, 55（7）：12861295.
[22]Hubbart S, Ajigboye O O, Horton P, et al. The photoprotective protein PsbS exerts control over CO2 assimilation rate in fluctuating light in rice. Plant J, 2012, 71（3）：402412.
[23]Ruban A V. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature, 2007, 450（7169）：575578.
[24]Anderson J M, Horton P, Kim E H, et al. Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philosoph Trans Royal Soc B：Biol Sci, 2012, 367（1608）：35153524.
[25]Johnson M P, Goral T K, Duffy C D, et al. Photoprotective energy dissipation involves the reorganization of photosystem Ⅱ lightharvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell Online, 2011, 23（4）：14681479.
[26]Goral T K, Johnson M P, Brain A P, et al. Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes：Effects of photoinhibition and protein phosphorylation. Plant J, 2010, 62（6）：948959.
[27]Johnson G, Young A, Horton P. Activation of nonphotochemical quenching in thylakoids and leaves. Planta, 1994, 194（4）：550556.
[28]Kramer D M, Cruz JA, KanazawaA. Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci, 2003, 8（1）：2732.
[29]Vaz J, Sharma P K. Relationship between xanthophyll cycle and nonphotochemical quenching in rice （Oryza sativa L. ）plants in response to light stress. Ind J Exp Biol, 2011, 49：6067.
[30]Zhou Y, Lam H M, Zhang J. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot, 2007, 58（5）：12071217.
[31]Thayer SS, Bjrkman O. Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosyn Res, 1990, 23（3）：331343.
[32]Miyake C, Miyata M, Shinzaki Y, et al. CO2 Response of cyclic electron flow around PSI (CEFPSI) in tobacco leaves—relative electron fluxes through PSⅠand PSⅡ determine the magnitude of nonphotochemical quenching (NPQ) of chl fluorescence. Plant Cell Physiol, 2005, 46（4）：629637.
[33]DemmigAdams B, Adams WW. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci, 1996, 1（1）：2126.
[34]Horton P, Ruban A V, Young A J. Regulation of the structure and function of the light harvesting complexes of photosystem II by the xanthophyll cycle. Photochem Carot, 1999：271291.
[35]Chen L S, Cheng L. Both xanthophyll cycledependent thermal dissipation and the antioxidant system are upregulated in grape（Vitis labrusca L. cv. Concord）leaves in response to N limitation. J Exp Bot, 2003, 54（390）：21652175.
[36]Cheng L. Xanthophyll cycle pool size and composition in relation to the nitrogen content of apple leaves. J Exp Bot, 2003, 54（381）：385393.
[37]Ji B, Jiao D. Relationships between D1 protein, xanthophyll cycle and photodamageresistant capacity in rice （Orysa sativa L. ）. Chin Sci Bull, 2000, 45（17）：15691575.
[38]Yin Y, Li S, Liao W, et al. Photosystem Ⅱ photochemistry, photoinhibition, and the xanthophyll cycle in heatstressed rice leaves. J Plant Physiol, 2010, 167（12）：959966.
[39]Quaas T, Berteotti S, Ballottari M, et al. Nonphotochemical quenching and xanthophyll cycle activities in six green algal species suggest mechanistic differences in the process of excess energy dissipation. J Plant Physiol, 2015, 172：92103.
[40]Roach T, Miller R, Aigner S, et al. Diurnal changes in the xanthophyll cycle pigments of freshwater algae correlate with the environmental hydrogen peroxide concentration rather than nonphotochemical quenching. Ann Bot, 2015, 116（4）：519527.
[41]Jahns P, Holzwarth A R. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys. Acta (BBA)Bioenergetics, 2012, 1817（1）：182193.
[42]Leverenz R L, Sutter M, Wilson A, et al. A 12  carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science, 2015, 348（6242）：14631466.
[43]Kirilovsky D. Modulating energy arriving at photochemical reaction centers: Orange carotenoid proteinrelated photoprotection and state transitions. Photosyn Res, 2015, 126（1）：317.
[44]DemmigAdams B, AdamsW W. Photosynthesis：Harvesting sunlight safely. Nature, 2000, 403（6768）：371374.
[45]Li X P, Gilmore A M, Caffarri S, et al. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem, 2004, 279（22）：2286622874.
[46]Ballottari M, Truong T B, De R E, et al. Identification of pHsensing sites in the light harvesting complex stressrelated 3 protein essential for triggering nonphotochemical quenching in Chlamydomonas reinhardtii. J Biol Chem, 2016：p. jbc. M115. 704601.
[47]Brooks M D, Jansson S, NiyogiK K, et al. PGRL1mediated cyclic electron flow is crucial for acclimation to anoxia and complementary to nonphotochemical quenching in tress adaptation. Plant Physiol, 2014: p. pp. 114.240648.
[48]Naranjo B, Mignée C, KriegerL A, et al. The chloroplast NADPH thioredoxin reductase C, NTRC, controls nonphotochemical quenching of light energy and photosynthetic electron transport in Arabidopsis. Plant, Cell Environ, 2015, p. pce. 12652.
[49]许大全. 植物光合机构的光破坏防御. 科学, 2002, 54（1）：1620.
Xu D Q. Photoprotection of plant photosynthetic organism. Science, 2002, 54（1）：1620(in Chinese with English abstract).
[50]DemmigAdams B. Nonphotochemical fluorescence quenching in contrasting plant species and environments. NonPhotochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Dordrecht, Springer, 2014：520550.
[51]Liu J Y, Qiu B S, Liu Z L, et al. Diurnal photosynthesis and photoinhibition of rice leaves with chlorophyll fluorescence. Acta Bot SinEnglish Ed, 2004, 46（5）：552559.
[52]Ishida S, Uebayashi N, Tazoe Y, et al. Diurnal and developmental changes in energy allocation of absorbed light at PSⅡ in fieldgrown rice. Plant Cell Physiol, 2014, 55（1）：171182.
[53]Ware M A, Belgio E, Ruban AV. Photoprotective capacity of nonphotochemical quenching in plants acclimated to different light intensities. Photosyn Res. 2015, 126：261–274.
[54]Lambrev P H, Miloslavina Y, Jahns P, et al. On the relationship between nonphotochemical quenching and photoprotection of Photosystem II. Biochim Biophy Acta, 2012, 1817：760–769.
[55]Ruban A V, Belgio E. The relationship between maximum tolerated light intensity and photoprotective energy dissipation in the photosynthetic antenna：Chloroplast gains and losses. Philosoph Trans Royal Soc B：Biol Sci, 2014, 369（1640）：1322.
[56]Ware M A, Belgio E, Ruban A V. Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. J Exp Bot, 2014：477489.
[57]许大全. 光合作用学, 北京：科学出版社, 2013：191199.
Xu D Q. The science of photosynthesis. Beijing：Science Press, 2013：191199(in Chinese with English abstract).
[58]Pospíil P. Production of reactive oxygen species by photosystem II. Biochim et Biophysica Acta （BBA）Bioenergetics, 2009, 1787（10）：11511160.
[59]Mohammad A H, Soumen B, Armin S M, et al. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance：Insights from ROS detoxification and scavenging. Fron Plant Sci. 2015, 6：119.
[60]Takahashi S, Badger M R. Photoprotection in plants：A new light on photosystem II damage. Trends Plant Sci, 2011, 16（1）：5360.
[61]Rochaix J D. Regulation and dynamics of the lightharvesting system. Ann Rev Plant Biol, 2014, 65：287309.
[62]Horton P, Johnson M P, PerezBueno M L, et al. Photosynthetic acclimation： Does the dynamic structure and macroorganisation of photosystem Ⅱ in higher plant grana membranes regulate light harvesting states. FEBS J, 2008, 275（6）：10691079.
[63]Giuliano G, Tavazza R, Diretto G, et al. Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotech, 2008, 26（3）：139145.
[64]Davison P, Hunter C, Horton P. Overexpression of βcarotene hydroxylase enhances stress tolerance in Arabidopsis. Nature, 2002, 418（6894）：203206.
[65]Ishida S, Morita K, Kishine M, et al. Allocation of absorbed light energy in PSⅡ to thermal dissipations in the presence or absence of PsbS subunits of rice. Plant Cell Physiol, 2011, 52（10）：18221831.
[66]Zulfugarov I S, Tovuu A, Eu Y J, et al. Production of superoxide from Photosystem II in a rice（Oryza sativa L. ）mutant lacking PsbS. BMC Plant Biol, 2014, 14（1）：242253.
[67]Xu C C, Jeon Y A, Lee C H. Relative contributions of photochemical and nonphotochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. Physiol Plant, 1999, 107（4）：447453.
[68]Wise R. Chillingenhanced photooxidation：The production, action and study of reactive oxygen species produced during chilling in the light. Photosyn Res, 1995, 45（2）：7997.
[69]Zhang Y, Chen L, He J, et al. Characteristics of chlorophyll fluorescence and antioxidative system in superhybrid rice and its parental cultivars under chilling stress. Biol Plant, 2010, 54（1）： 164168.
[70]Hirotsu N, Makino A, Ushio A, et al. 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 Physiol, 2004, 45（5）：635644.
[71]Bonnecarrère V, Borsani O, Díaz P, et al. Response to photoxidative stress induced by cold in japonica rice is genotype dependent. Plant Sci, 2011, 180（5）：726732.
[72]Wada S, Hayashida Y, Izumi M, et al. Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice. Plant Physiol, 2015, 168（1）：6073.
[73]Gu J, Yin X, Stomph T J, et al. Can exploiting natural genetic variation in leaf photosynthesis contribute to increasing rice productivity? A simulation analysis. Plant, Cell Environ, 2014, 37（1）：2234.
[74]Xu G H, Fan X R, Miller A J. Plant nitrogen assimilation and use efficiency. Ann Rev Plant Biol, 2012, 63：153182.
[75]Makino A, Sato T, Nakano H, et al. Leaf photosynthesis, plant growth and nitrogen allocation in rice under different irradiances. Planta, 1997, 203（3）：390398.
[76]Kanemura T, Homma K, Ohsumi A, et al. Evaluation of genotypic variation in leaf photosynthetic rate and its associated factors by using rice diversity research set of germplasm. Photosyn Res, 2007, 94（1）： 2330.
[77]Kumagai E, Araki T, Kubota F. Characteristics of gas exchange and chlorophyll fluorescence during senescence of flag leaf in different rice（Oryza sativa L. ）cultivars grown under nitrogendeficient condition. Plant Prod Sci, 2009, 12（3）：285292.
[78]Huang Z A, Jiang D A, Yang Y, et al. Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants. Photosynthetica, 2004, 42（3）：357364.
[79]Evans J, Poorter H. Photosynthetic acclimation of plants to growth irradiance：The relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell Environ, 2001, 24（8）：755767.
[80]Makino A, Nakano H, Mae T. Responses of ribulose1, 5bisphosphate carboxylase, cytochrome f, and sucrose synthesis enzymes in rice leaves to leaf nitrogen and their relationships to photosynthesis. Plant Physiol, 1994, 105（1）：173179.
[81]Evans J R. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia, 1989, 78（1）：919.
[82]王仁雷, 华春, 魏锦城. 氮水平对水稻汕优64和金南风光合特性的影响. 中国水稻科学, 2002, 16（4）：331334.
Wang R L, Hua C, Wei J C, et al. Effect of nitrogen levels on photosynthetic characteristics of rice variety(combination) Shanyou 64 and Kinmaze. Chin J Rice Sci, 2002, 16（4）：331334. (in Chinese with English abstract).
[83]李勇. 氮素营养对水稻光合作用与光合氮素利用率的影响机制研究. 南京：南京农业大学, 2013.
Li Y. Studies on mechanisms of the effects of different nitrogen supplies on photosynthesis and photosynthetic nitrogen use efficiency of rice plants. Nanjing：Nanjing Agricultural University. 2013.
[84]Long J, Ma G, Wan Y, et al. Effects of nitrogen fertilizer level on chlorophyll fluorescence characteristics in flag leaf of super hybrid rice at late growth stage. Rice Sci, 2013, 20（3）：220228.
[85]Li Y, Yang X, Ren B, et al. Why nitrogen use efficiency decreases under high nitrogen supply in rice （Oryza sativa L. ）seedlings. J Plant Growth Reg, 2012, 31（1）：4752.
[86]Shrestha S, Brueck H, Asch F. Chlorophyll index, photochemical reflectance index and chlorophyll fluorescence measurements of rice leaves supplied with different N levels. J Photochem Photobiol B：Biology, 2012, 113：713.
[87]Du H, Wang N, Cui F, et al. Characterization of the βcarotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol, 2010, 154（3）：13041318.
[88]Pieters A J, El Souki S. Effects of drought during grain filling on PS II activity in rice. J Plant Physiol, 2005, 162（8）：903911.
[89]Chaves M, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress：Regulation mechanisms from whole plant to cell. Ann Bot, 2009, 103（4）：551560.
[90]Moradi F, Ismail A M. Responses of photosynthesis, chlorophyll fluorescence and ROSscavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot, 2007, 99（6）：11611173.
[91]Zhu S Q, Chen M W, Ji B H, et al. Roles of xanthophylls and exogenous ABA in protection against NaClinduced photodamage in rice （Oryza sativa L）and cabbage（Brassica campestris）. J Exp Bot, 2011, 62（13）：46174625.
[92]Fang J, Chai C, Qian Q, et al. Mutations of genes in synthesis of the carotenoid precursors of ABA lead to preharvest sprouting and photooxidation in rice. Plant J, 2008, 54（2）：177189.
[93]Erik H, Murchie Y C, Hubbart S, et al. Interactions between Senescence and Leaf Orientation Determine in Situ Patterns of Photosynthesis and Photoinhibition in FieldGrown Rice. Plant Physiol, 1999：553563.
[94]Long S P, Amy M C, Zhu X G. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell, 2015, 161（1）：5666.
[95]Peng S, Khush G S, Virk P, et al. Progress in ideotype breeding to increase rice yield potential. Field Crops Res, 2008, 108（1）：3238.
[96]Ye N, Jia L, Zhang J. ABA signal in rice under stress conditions. Rice, 2012, 5（1）：19.
[97]Peter H, Stephen G T. Gibberellin biosynthesis and its regulation. Biochem J, 2012, 444（1）：1125.
[98]Hoffmann B S, Kende H. The role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol, 1992, 99（3）：11561161.
[99]Cheminant S, Wild M, Bouvier F, et al. DELLAs regulate chlorophyll and carotenoid biosynthesis to prevent photooxidative damage during seedling deetiolation in Arabidopsis. Plant Cell Online, 2011, 23（5）：18491860.
[100]Qin G, Gu H, Ma L, et al. Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Res, 2007, 17（5）：471482.
[101]Duan H K, Yan Z, Qi D, et al. Comparative study on the expression of genes involved in carotenoid and ABA biosynthetic pathway in response to salt stress in tomato. J Integr Agric, 2012, 11（7）：10931102.