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Acta Agron Sin ›› 2018, Vol. 44 ›› Issue (01): 82-94.doi: 10.3724/SP.J.1006.2018.00082

• TILLAGE & CULTIVATION·PHYSIOLOGY & BIOCHEMISTRY • Previous Articles     Next Articles

Physiological Mechanism on Drought Tolerance Enhanced by Exogenous Glucose in C4-pepc Rice

ZHANG Jin-Fei1, 2, LI Xia1,*, HE Ya-Fei1, 2,XIE Yin-Feng2   

  1. 1 Institute of Food Crops, Jiangsu Rice Engineering Research Center, National Center for Rice Improvement (Nanjing), Jiangsu Academy of Agricultural Sciences, Nanjing 210014, Jiangsu, China; 2 College of Biology and Environment, Nanjing Forestry University, Nanjing 210037, Jiangsu, China
  • Received:2017-03-28 Revised:2017-09-10 Online:2018-01-12 Published:2017-09-28
  • Contact: 李霞, E-mail: jspplx@jaas.ac.cn E-mail:820788317@qq.com
  • Supported by:

    This study was supported by the National Natural Science Foundation of China (31571585), the Jiangsu Provincial Academy of Agricultural Sciences Basic Research Business Special Project (ZX [16] 2002), and the Grant from the Institute of Food Crops of Jiangsu Academy of Agricultural Sciences (LZS17-9).

Abstract:

In order to investigate the intrinsic mechanism of glucose participated in drought tolerance in plants, the effects of glucose were studied using the phosphoenolpyruvate carboxylase (C4-pepc) rice (PC) and “Kitaake” (WT) rice lines in pot experiments and hydroponics experiments respectively. The changes of photosynthetic parameters, total soluble sugar and sugar components contents, Ca2+ and NO contents, hexokinase activity, transcript levels of sucrose nonfermenting-1(SNF1)-related protein kinases 3 (SnRK3s) and calcitonin B-like (CBL) of the functional leaves in rice lines were measured. Agronomic traits of the wild type (WT) and PC were recorded in the mature period. In pot experiment, the treatment of 3% glucose with drought during tillering stage had no significant effect on agronomic traits of the tested rice. During the booting stage, the plant height, panicle number per plant, filled grain number per panicle and grain yield per plant in PC were significantly higher than in WT (P < 0.05). In the hydroponics experiment with 1% glucose combined with 12% (m/v) polyethylene glycol 6000 (PEG-6000) to simulate drought stress, the photosynthetic parameters such as net photosynthetic rate (Pn), stomatal conductance (Gs) and carboxylation efficiency (Ce) significantly increased in PC than in WT. Similarly, the contents of sucrose and fructose of leaves in PC lines were significantly higher than those in WT. It was noteworthy that hexokinase (HXK) activity and the relative gene expression of CBL and SnRK3.1/SnRK3.4/SnRK3.21 in PC lines under the treatment with 1% glucose and 12% PEG were significantly lower than those under 12% PEG treatment alone. Intriguingly, the NO contents of PC under the corresponding treatments were significantly increased (P < 0.05). In addition, the photosynthetic parameters were significantly correlated with the glucose content, HXK activity and SnRK3.16 transcript level respectively in PC lines. It is suggested that PC can decrease the expression of CBL and SnRK3s gene by increasing glucose, participate the stomatal regulation via NO, maintain relative water content, keep stable photosynthetic capacity, and therefore confer drought tolerance.

Key words: rice, glucose, phosphate phosphoenolpyruvate carboxylase, stomatal conductance, drought

[1] Khush G S. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol, 2005, 59: 1–6 [2] Todaka D, Shinozaki K, Yamaguchi-Shinozaki K. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci, 2015, 6: 84 [3] Long S P, Marshall-Colon A, Zhu X G. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell, 2015, 161: 56–66 [4] Aubry S, Brown N J, Hibberd J M. The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot, 2011, 62: 3049–3059 [5] Ku M S B, Agarie S, Nomura M, Fukayama H, Tsuchida H, Ono K, Hirose S, Toki S, Miyao M, Matsuoka M. High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nat Biotechnol, 1999, 17: 76–80 [6] Orta D R, Merchant S S, Alric J, Barkan A, Blankenship R E, Bock R, Moore T A. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA, 2015, 112: 8529–8536 [7] Johnson J F, Vance C P, Allan D L. Phosphorus deficiency in Lupinus albus altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol, 1996, 112: 31–41 [8] Chen P B, Li X, Huo K, Wei X D, Dai C C, Lu C G. Promotion of photosynthesis in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene by nitric oxide donors. J Plant Physiol, 2014, 171: 458–466 [9] Ren C G, Li X, Liu X L, Wei X D, Dai C C. Hydrogen peroxide regulated photosynthesis in C4-pepc transgenic rice. Plant Physiol Biochem, 2014, 74: 218–229 [10] 方立锋, 丁在松, 赵明. 转ppc基因水稻苗期抗旱特性研究. 作物学报, 2008, 34: 1220–1226 Fang L F, Ding Z S, Zhao M. Characteristics of drought tolerance in ppc overexpressed rice seedlings. Acta Agron Sin, 2008, 34: 1220–1226 (in Chinese with English abstract) [11] Qian B, Li X, Liu X, Wang M. Improved oxidative tolerance in suspension cultured cells of C4-pepc transgenic rice by H2O2 and Ca2+ under PEG-6000. J Integr Plant Biol, 2015, 57: 534–549 [12] 周宝元, 丁在松, 赵明. PEPC过表达可以减轻干旱胁迫对水稻光合的抑制作用. 作物学报, 2011, 37: 112–118 Zhou B Y, Ding Z S, Zhao M. Alleviation of drought stress inhibition on photosynthesis by overexpression of PEPC gene in rice. Acta Agron Sin, 2011, 37: 112–118 (in Chinese with English abstract) [13] 丁在松, 周宝元, 孙雪芳, 赵明. 干旱胁迫下PEPC过表达增强水稻的耐强光能力. 作物学报, 2012, 38: 285–292 Ding Z S, Zhou B Y, Sun X F, Zhao M. High light tolerance is enhanced by overexpressed PEPC in rice under drought stress. Acta Agron Sin, 2012, 38: 285–292 (in Chinese with English abstract) [14] Vavasseur A, Raghavendra A S. Guard cell metabolism and CO2 sensing. New Phytol, 2005, 16: 665–682 [15] Liu X L, Li X, Zhang C, Dai C C, Zhou J Y, Ren C G, Zhang J F. Phosphoenolpyruvate carboxylase regulation in C4-PEPC expressing transgenic rice during early responses to drought stress. Physiol Plant, 2017, 159: 178–200 [16] Li L, Sheen J. Dynamic and diverse sugar signaling. Curr Opin Plant Biol, 2016, 33: 116–125 [17] Moore B, Zhou L, Rolland F, Hall Q, Cheng W H, Liu Y X, Hwang I, Jones T, Sheen J. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science, 2003, 300: 332–336 [18] Kelly G, David-Schartz R, Sade N, Moshelion M, Levi A, Alchanatis V, Granot D. The pitfalls of transgenic selection and new roles of AtHXK1: a high level of AtHXK1 expression uncouples hexokinas1-dependent sugar signaling from exogenous sugar. Plant Physiol, 2012, 159: 47–51 [19] Kim Y M, Heinzel N, Giese J O, Koeber J, Melzer M, Rutten T, Wiren N, Sonnewald U, Hajirezaei M R. A dual role of tobacco hexokinase1 in primary metabolism and sugar sensing. Plant Cell Environ, 2013, 36: 1311–1327 [20] Considine M J, Foyer C H. Redox regulation of plant development. Antioxid Redox Signal, 2014, 21: 1305–1326 [21] Matsoukas I G. Interplay between sugar and hormone signaling pathways modulate floral signal transduction. Front Genet, 2014, 5: 218 [22] Tsai A Y, Gazzarrini S. Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture. Front Plant Sci, 2014, 5: 119 [23] Jung K, Nemhauser J L, Perata P. New mechanistic links between sugar and hormone signalling networks. Curr Opin Plant Biol, 2015, 25: 130–137 [24] Yu S, Lian H, Wang J W. Plant development transitions: the role of microRNAs and sugars. Curr Opin Plant Biol, 2015, 27: 1–7 [25] Sheen J. Master regulators in plant glucose signaling networks. J Plant Biol, 2014, 57: 67–79 [26] Zhang Z W, Yaun S, Xu F, Yang H, Zhang N H, Cheng J, Lin H H. The plastid hexokinase pHXK: a node of convergence for sugar and plastid signals in Arabidopsis. FEBS Lett, 2010, 584: 3573–3579 [27] Hanson J, Smeekens S. Sugar perception and signaling: an update. Curr Opin Plant Biol, 2009, 12: 562–567 [28] Toroser D, Plaut Z, Huber S C. Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiol, 2000, 123: 403–412 [29] Zhang Y, Primavesi L F, Jhurreea D, Andraloj P J, Mitchell R A C, Powers S J, Schluepmann H, Delatte T, Wingler A, Paul M J. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol, 2009, 149: 1860–1871 [30] Li X, Wang C. Physiological and metabolic enzymes activity changes in transgenic rice plants with increased phosphoenolpyruvate carboxylase activity during the flowering stage. Acta Physiol Plant, 2013, 35: 1503–1512 [31] Doubnerová V, Ry?lavá H. What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci, 2011, 180: 575–583 [32] Yoshida S, Forno D A, Cock J H. Laboratory Manual for Physiological Studies of Rice. Philippines: International Rice Research Institute, 1976. pp 61–64 [33] Smart R E, Bingham G E. Rapid estimates of relative water-content. Plant Physiol, 1974, 53: 258–260 [34] Ambavaram, M M, Basu S, Krishnan A, Ramegowda V, Batlang U, Rahman L, Pereira A. Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat Commun, 2014, 5: 93 [35] Li X, Wang C, Ren C G. Effects of 1-butanol, neomycin and calcium on the photosynthetic characteristics of pepc transgenic rice. Afr J Biol Technol, 2011, 10: 17466–17476 [36] Yang C Q, Liu W N, Zhao Z H, Wu H Y. Determination of the content of serum calcium with methylthymol blue as chromogenic reagent. Spectrosc Spectr Anal, 1998, 18: 485–487 [37] Murphy M E, Noack E. Nitric oxide assay using hemoglobin method. Methods Enzymol, 1994, 233: 240–250 [38] Schaffer A A, Petreikov M. Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol, 1997, 113: 739–746 [39] Jung H, Kim J K, Ha S W. Use of animal viral IRES sequence makes multiple truncated transcripts without mediating polycistronic expression in rice. J Korean Soc Biol Chem, 2011, 54: 678–684 [40] Izui K, Matsumura H, Furumoto T, Kai Y. Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu Rev Plant Physiol, 2004, 55: 69–84 [41] Sethi D, Dash S, Mohapatra S, Mohanty P. C4 rice: an advance technique for enhancing rice production. Adv Life Sci, 2016, 5: 2535–2542 [42] 吴琼, 许为钢, 李艳, 齐学礼, 胡琳, 张磊, 韩琳琳. 田间条件下转玉米C4型PEPC基因小麦的光合生理特性. 作物学报, 2010, 37: 2046–2052 Wu Q, Xu W G, Li Y, Qi X L, Hu L, Zhang L, Han L L. Physiological characteristics of photosynthesis in transgenic wheat with maize C4-PEPC gene under field conditions. Acta Agron Sin, 2010, 37: 2046–2052 (in Chinese with English abstract) [43] Karaba A, Dixit S, Greco R, Aharoni A, Trijatmiko K R, Marsch-Martinez N, Pereira A. Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Nat Aca Sci USA, 2007, 104: 15270–15275 [44] Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H J, Rosenkranz R, Peterh?nsel C. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol, 2007, 25: 593–599 [45] Abebe T, Guenzi A C, Martin B, Cushman J C. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol, 2003, 131: 1748–1755 [46] Daloso D M, Anjos L, Fernie A R. Roles of sucrose in guard cell regulation. New Phytol, 2016, 211: 809 [47] Granot D, Lugassi N, Kottapalli J, Kelly G. Sensing sugar and saving water. Proc Environ Sci, 2015, 29: 3 [48] Griffiths C A, Sagar R, Geng Y, Primavesi L F, Patel M K, Passarelli M K, Davis B G. Chemical intervention in plant sugar signaling increases yield and resilience. Nature, 2016, 540: 574–578 [49] Corpas F J, Barroso J B. Peroxisomal plant metabolism–an update on nitric oxide, Ca2+ and the NADPH recycling network. J Cell Sci, 2017, jcs. 202978. [50] Furuichi T, Cunningham K W, Muto S. A putative two pore channel AtTPC1 mediates Ca2+ flux in Arabidopsis leaf cells. Plant Cell Physiol, 2001, 42: 900–905 [51] Li Z Y, Xu Z S, Chen Y, He G Y, Yang G X, Chen M, Ma Y Z. A novel role for Arabidopsis CBL1 in affecting plant responses to glucose and gibberellin during germination and seedling development. PLoS One, 2013, 8: e56412 [52] Batistic O, Kudla J. Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophys Acta, 2009, 1790: 985–992 [53]T ominaga M, Harada A, Kinoshita T, Shimazaki K. Biochemical characterization of calcineurin B-like-interacting protein kinase in Vicia guard cells. Plant Cell Physiol, 2010, 51: 408–421 [54] Mao J, Manik S M, Shi S, Chao J, Jin Y, Wang Q, Liu H. Mechanisms and physiological roles of the CBL-CIPK networking system in Arabidopsis thaliana. Genes, 2016, 7: 62 [55] Li J, Long Y, Qi G N, Xu Z J, Wu W H, Wang Y. The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex. Plant Cell, 2014, 26: 3387-3402. [56] Kudahettige N P, Pucciariello C, Parlanti S, Alpi A, Perata P. Regulatory interplay of the Sub1A and CIPK15 pathways in the regulation of α-amylase production in flooded rice plants. Plant Biol, 2011, 13: 611–619.
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