Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (8): 1532-1544.doi: 10.3864/j.issn.0578-1752.2020.08.004

• TILLAGE & CULTIVATION·PHYSIOLOGY & BIOCHEMISTRY·AGRICULTURE INFORMATION TECHNOLOGY • Previous Articles     Next Articles

Response of Non-Photochemical Quenching in Bundle Sheath Chloroplasts of Two Maize Hybrids to Drought Stress

LIU WenJuan1,CHANG LiJuan1,YUE LiJie2,SONG Jun1,ZHANG FuLi1,WANG Dong1,WU JiaWei1,GUO LingAn1,LEI ShaoRong1   

  1. 1 Center of Analysis and Testing, Sichuan Academy of Agricultural Sciences, Chengdu 610066
    2 Crop Research Institute, Sichuan Academy of Agricultural Sciences, Chengdu 610066
  • Received:2019-09-04 Accepted:2019-12-11 Online:2020-04-16 Published:2020-04-29

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Abstract:

【Objective】 Non-photochemical chlorophyll fluorescence quenching (NPQ) of photosystem II (PSII) is the most rapid photoprotective mechanism of higher plants that responds to a changing environment. Maize has two distinctly different classes of chloroplasts in mesophyll and bundle sheath cells. In the present study, the drought tolerance of two maize hybrids was compared to explore the significance of non-photochemical quenching in bundle sheath chloroplasts to maize tolerance. 【Method】 The experiment was conducted with two maize hybrids, Chengdan 30 and Zhongyu 3, and consisted of three soil moisture regimes, including 70%-80% of field water capacity (FWC) (sufficient irrigation), 50%-60% FWC (moderate drought stress), and 35%-45% FWC (severe drought stress). Physiological and biochemical parameters of maize leaves, including relative water content, chlorophyll contents, reactive oxygen species (ROS) accumulation, lipid peroxidation, and gas exchange, were measured. Fv/Fm and NPQ of PSII in mesophyll and bundle sheath chloroplasts of two maize hybrids were investigated through a chlorophyll fluorescence kinetic microscope. The steady-state levels of PSII subunit S (PsbS) in mesophyll and bundle sheath cells were analyzed using method of western blotting. PSII complexes levels were detected by blue native PAGE. 【Result】 The stomatal conductance and transpiration rate of maize leaves decreased under drought stress. There were no remarkably difference in decline degree of stomatal index between Chengdan 30 and Zhongyu 3. However, under severe drought conditions, Chengdan 30 showed better leaf water status, lower ROS damages, and higher photosynthetic efficiency compared with Zhongyu 3. NPQ levels and PsbS contents in bundle sheath chloroplasts increased more markedly than that in mesophyll chloroplasts when maize plant suffered with drought treatment, which was especially outstanding in Chengdan 30. The PSII complexes contents of Zhongyu 3 reduced obviously under drought stress, while the steady-state levels of light-harvesting complex II (LHCII) trimer of Chengdan 30 enhanced after severe drought. 【Conclusion】 The responses of photosynthetic mechanism to stomatal limitation were no significant difference in two maize hybrids under drought stress. However, compared with Zhongyu 3, Chengdan 30 had a higher non-photochemical quenching capacity in bundle sheath chloroplasts, which might play a positive influence on its superior drought tolerance of non-stomatal limitation.

Key words: maize, drought stress, bundle sheath cells, photosystem II, non-photochemical quenching

Fig. 1

Leaf water status and lipid peroxidation in maize leaves under drought stress A: Plant phenotypes observation; B: Relative water content (RWC); C: Chlorophyll a and b contents (Chl a+b); D: Superoxide anion radicals (O2-) content; E: Hydrogen peroxide (H2O2) content; F: Electrolyte leakage; G: Malondialdehyde (MDA) content. CK, well watered control; MS, moderate drought stress; SS, severe drought stress. Each point represents the mean±SD (n=4). Different letters indicate significant differences among one maize hybrid under progressive drought treatments at 0.05 level. One or two asterisks indicate significant differences between two maize hybrids under drought stress at P<0.05, and P<0.01, respectively. The same as below"

Fig. 2

Gas exchange in maize leaves under drought stress A: Stomatal conductance (gs); B: Transpiration rate (E); C: Intercellular CO2 concentration (Ci); D: Net photosynthetic rate (A)"

Fig. 3

Measurement of Fv/Fm in mesophyll and bundle sheath chloroplasts of maize leaves under drought stress A: Imaging of Fv/Fm in mesophyll and bundle sheath chloroplasts; B: Quantification of Fv/Fm in mesophyll and bundle sheath chloroplasts. M, mesophyll chloroplasts; BS, bundle sheath chloroplasts. The same as below"

Fig. 4

Measurement of NPQ in mesophyll and bundle sheath chloroplasts of maize leaves under drought stress A: Imaging of NPQ in mesophyll and bundle sheath chloroplasts; B: Quantification of NPQ in mesophyll and bundle sheath chloroplasts"

Fig. 5

Steady-state level of PsbS protein in mesophyll and bundle sheath cells of maize leaves under drought stress A: Immunoblot analyses of PsbS in mesophyll cells (1.0 μg Chl); B: Immunoblot analyses of PsbS in bundle sheath cells (1.5 μg Chl); C: Quantification of PsbS immunoblot signal in mesophyll cells (the amount of the PsbS protein in mesophyll cells of Chengdan 30 maize under well watered condition was defined as 100%); D: Quantification of PsbS immunoblot signal in bundle sheath cells (the amount of the PsbS protein in bundle sheath cells of Chengdan 30 maize under well watered condition was defined as 100%). Coomassie blue staining (CBS) of protein samples were shown as the control"

Fig. 6

Steady-state levels of PSII complexes in mesophyll and bundle sheath cells of maize leaves under drought stress A: Membranes in mesophyll thylakoids were solubilized with 1% DDM and loaded onto 4%-12% acrylamide Blue-Native gel; B: Membranes in bundle sheath thylakoids were solubilized with 2% DDM and loaded onto 4%-12% acrylamide Blue-Native gel; C: Quantification of LHCII trimer in mesophyll thylakoids (the amount of the LHCII trimer under well watered condition was defined as 100%); D: Quantification of LHCII trimer in bundle sheath thylakoids (the amount of the LHCII trimer under well watered condition was defined as 100%)"

[1] YUAN S, LIU W J, ZHANG N H, WANG M B, LIANG H G, LIN H H . Effects of water stress on major PSII gene expression and protein metabolism in barley leaves. Physiologia Plantarum, 2005,125(4):464-473.
[2] LIU W J, CHEN Y E, TIAN W J, DU J B, ZHANG Z W, XU F, ZHANG F, YUAN S, LIN H H . Dephosphorylation of photosystem II proteins and phosphorylation of CP29 in barley photosynthetic membranes as a response to water stress. Biochimica et Biophysica Acta-Bioenergetics, 2009,1787(10):1238-1245.
[3] CAMPOSA H, TREJOB C, PEÑA-VALDIVIA C B, GARCIA-NAVA R, CONDE-MARTINEZ F V, CRUZ-ORTEGA M R . Stomatal and non-stomatal limitations of bell pepper ( Capsicum annuum L.) plants under water stress and re-watering: Delayed restoration of photosynthesis during recovery. Environmental and Experimental Botany, 2014,98(1):56-64.
[4] KRAMER D M, EVANS J R . The importance of energy balance in improving photosynthetic productivity. Plant Physiology, 2011,155(1):70-78.
[5] TIKKANEN M, ARO E M . Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochimica et Biophysica Acta-Bioenergetics, 2012,1817(1):232-238.
[6] KROMDIJK J, GLOWACKA K, LEONELLI L, GABILLY S T, IWAI M, NIYOGI K K, LONG S P . Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 2016,354(6314):857-861.
[7] GRIFFITHS H, PARRY M . Plant responses to water stress. Annals of Botany, 2002,89(7):801-802.
[8] CHEN Y E, LIU W J, SU Y Q, CUI J M, ZHANG Z W, YUAN M, ZHANG H Y, YUAN S . Different response of photosystem II to short and long term drought stress in Arabidopsis thaliana. Physiologia Plantarum, 2016,158(2):225-235.
[9] VIRGIN H I . Chlorophyll formation and water deficit. Physiologic Plantarum, 1965,18(4):994-1000.
[10] BAENA-GONZALEZ E, BARBATO R, ARO E M . Role of phosphorylation in the repair cycle and oligomeric structure of photosystem II. Planta, 1999,208(2):196-204.
[11] LIU W J, YUAN S, ZHANG N H, LEI T, DUAN H G, LIANG H G, LIN H H . Effect of water stress on photosystem 2 in two wheat cultivars. Biologia Plantarum, 2006,50(4):597-602.
[12] 张仁和, 郑友军, 马国胜, 张兴华, 路海东, 史俊通, 薛吉全 . 干旱胁迫对玉米苗期叶片光合作用和保护酶活性的影响. 生态学报, 2011,31(5):1303-1311.
ZHANG R H, ZHENG Y J, MA G S, ZHANG X H, LU H D, SHI J T, XUE J Q . Effect of drought stress on photosynthetic traits and protective enzyme activity in maize seeding. Acta Ecologica Sinica, 2011,31(5):1303-1311. (in Chinese)
[13] CHEN Y E, SU Y Q, ZHANG C M, MA J, MAO H T, YANG Z H, YUAN M, ZHANG Z W, YUAN S, Zhang H Y . Comparison of photosynthetic characteristics and antioxidant systems in different wheat strains. Journal of Plant Growth Regulation, 2018,37(2):347-359.
[14] ROMANOWSKA E, DROZAK A, POKORSKA B, SHIELL B J, MICHALSKI W P . Organization and activity of photosystems in the mesophyll and bundle sheath chloroplasts of maize. Journal of Plant Physiology, 2006,163(6):607-618.
[15] ROMANOWSKA E, KARGUL J, POWIKROWSKA M, FINAZZI G, NIELD J, DROZAK A, POKORSKA B . Structural organization of photosynthetic apparatus in agranal chloroplasts of maize. Journal of Biological Chemistry, 2008,283(38):26037-26046.
[16] POKORSKA B, ZIENKIEWICZ M, POWIKROWSKA M, DROZAK A, ROMANOWSKA E . Differential turnover of the photosystem II reaction centre D1 protein in mesophyll and bundle sheath chloroplasts of maize. Biochimica et Biophysica Acta-Bioenergetics, 2009,1787(10):1161-1169.
[17] 裴英杰, 郑家玲, 庾红, 王金胜, 丁起盛, 郭栋生, 郭春绒 . 用于玉米品种抗旱性鉴定的生理生化指标. 华北农学报, 1992,7(1):31-35.
PEI Y J, ZHENG J L, YU H, WANG J S, DING Q S, GUO D S, GUO C R . The indexes of physiology and biochemistry used for appraisal and level determination of drought resistance in maize. Acta Agriculturae Boreali-Sinica, 1992,7(1):31-35. (in Chinese)
[18] 郭艳阳, 刘佳, 朱亚利, 柏延文, 李红杰, 薛吉全, 张仁和 . 玉米叶片光合和抗氧化酶活性对干旱胁迫的响应. 植物生理学报, 2018,54(12):1839-1846.
GUO Y Y, LIU J, ZHU Y L, BAI Y W, LI H J, XUE J Q, ZHANG R H . Responses of photosynthetic and antioxidant enzyme activities in maize leaves to drought stress. Plant Physiology Journal, 2018,54(12):1839-1846. (in Chinese)
[19] 刘亚, 丁俊强, 苏巴钱德, 廖登群, 赵久然, 李建生 . 基于远红外热成像的叶温变化与玉米苗期耐旱性的研究. 中国农业科学, 2009,42(6):2192-2201.
LIU Y, DING J Q, SUBHASH C, LIAO D Q, ZHAO J R, LI J S . Identification of maize drought-tolerance at seeding stage based on leaf temperature using infrared thermography. Scientia Agricultura Sinica, 2009,42(6):2192-2201. (in Chinese)
[20] 舒展, 张晓素, 陈娟, 陈根云, 许大全 . 叶绿素含量测定的简化. 植物生理学通讯, 2010,46(4):399-402.
SHU Z, ZHANG X S, CHEN J, CHEN G Y, XU D Q . The simplification of chlorophyll content measurement. Plant Physiology Communications, 2010,46(4):399-402. (in Chinese)
[21] ROMANOWSKA E, PARYS E . Mechanical isolation of bundle sheath cell strands and thylakoids from leaves of C4 grasses. Methods in Molecular Biology, 2011,684:327-337.
[22] WITTIG I, BRAUN H P, SCHÄGGER H . Blue native PAGE. Nature Protocols, 2006,1(1):418-428.
[23] FERIMAZOVA N, FELCMANOVÁ K, ŠETLÍKOVÁ E, KÜPPER H, MALDENER I, HAUSKA G, ŠEDIVÁ B, PRÁŠIL O . Regulation of photosynthesis during heterocyst differentiation in Anabaena sp. strain PCC 7120 investigated in vivo at single-cell level by chlorophyll fluorescence kinetic microscopy. Photosynthesis Research, 2013,116(1):79-91.
[24] GORECKA M, ALVAREZ-FERNANDEZ R, SLATTERY K, MCAUSLAND L, DAVEY P A, KARPINSKI S, LAWSON T, MULLINEAUX P M . Abscisic acid signalling determines susceptibility of bundle sheath cells to photoinhibition in high light-exposed Arabidopsis leaves. Philosophical Transactions of the Royal Society B Biological Sciences, 2014,369(1640):20130234.
[25] DUFFY C D P, RUBAN A V . Dissipative pathways in the photosystem-II antenna in plants. Journal of Photochemistry Photobiolgy B: Biology, 2015,152:215-226.
[26] RUBAN , ALEXANDER V . Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plants from photodamage. Plant Physiology, 2016,170(4):1903-1916.
[27] BALLOTTARI M, DALL'OSTO L, MOROSINOTTO T, BASSI R . Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. Journal of Biological Chemistry, 2007,282(12):8947-8958.
[28] ROACH T, KRIEGER-LISZKAY A . The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana. Biochimica et Biophysica Acta-Bioenergetics, 2012,1817(12):2158-2165.
[29] GLOWACKA K, KROMDIJK J, KUCERA K, XIE J Y, CAVANAGH A P, LEONELLI L, LEAKEY A D B, ORT D R, NIYOGI K K, LONG T P . Photosystem II ubnit S overexpression increases the efficiency of water use in a field-grown crop. Nature Communications, 2018,9(1):868.
[30] EL-SHARKAWY M A . Pioneering research on C4 leaf anatomical, physiological, and agronomic characteristics of tropical monocot and dicot plant species: Implications for crop water relations and productivity in comparison to C3 cropping systems. Photosynthetica, 2009,47(2):163-183.
[31] WARE M A, BELGIO E, RUBAN A V . Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. Journal of Experimental Botany, 2015,66(5):1259-1270.
[32] ZULFUGAROV I S, TOVUU A, EU Y J, DOGSOM B, POUDYAL R S, NATH K, HALL M, BANERJEE M, YOON U C, MOON Y H, AN G, JANSSON S, LEE C H . Production of superoxide from Photosystem II in a rice ( Oryza sativa L.) mutant lacking PsbS. BMC Plant Biology, 2014,14(1):242.
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