Physiological and biochemical characterization of NERICA-L-44: A novel source of heat tolerance at the vegetative and reproductive stages in rice

Physiologia Plantarum

Volumn 154, Issue 4, 2015, Pages 543-559

  Bahuguna, Rajeev N ^a,b   Jha, Jyoti ^a   Pal, Madan ^a   Shah, Divya ^a   Lawas, Lovely Mf ^b   Khetarpal, Sangeetha ^a   Jagadish, Krishna S V ^b  

^a INDIAN AGRICULTURAL RESEARCH INSTITUTE   (India)

^b INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CHLOROPHYLL; VEGETABLE PROTEIN;

ADAPTATION; FLOWER; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; ORYZA; OXIDATIVE STRESS; PHYSIOLOGY; REPRODUCTION;

ADAPTATION, PHYSIOLOGICAL; ANTIOXIDANTS; CHLOROPHYLL; FLOWERS; HOT TEMPERATURE; ORYZA; OXIDATIVE STRESS; PLANT PROTEINS; REPRODUCTION;

EID: 84937412976     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12299     Document Type: Article

References (81)

1. Adu-Kwarteng E, Ellis WO, Oduro I, Manful JT (2003) Rice grain quality: a comparison of local varieties with new varieties under study in Ghana. Food Control 14: 507-514
2. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24: 1337-1344
3. Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171: 382-388
4. Anderson JA, Padhye SR (2004) Protein aggregation, radical scavenging capacity, and stability of hydrogen peroxide defense systems in heat-stressed vinca and sweet pea leaves. J Amer Soc Hort Sci 129: 54-59
5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
6. Ara N, Nakkanong K, Lv W, Yang J, Hu Z, Zhang M (2013) Antioxidant enzymatic activities and gene expression associated with heat tolerance in the stems and roots of two Cucurbit species ("Cucurbita maxima" and "Cucurbita moschata") and their interspecific inbred line "Maxchata". Int J Mol Sci 14: 24008-24028
7. Ayeneh A, Van Ginkel M, Reynolds MP, Ammar K (2002) Comparison of leaf, spike, peduncle and canopy temperature depression in wheat under heat stress. Field Crops Res 79: 173-184
8. Battisti DS, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323: 240-244
9. Bhoomika K, Pyngrope S, Dubey RS (2013) Differential responses of antioxidant enzymes to aluminum toxicity in two rice (Oryza sativa L.) cultivars with marked presence and elevated activity of Fe SOD and enhanced activities of Mn SOD and catalase in aluminum tolerant cultivar. Plant Growth Regul 71: 235-252
10. Bonifacio A, Martins MO, Ribeiro CW, Fontenele AV, Carvalho FEL, Margis-Pinheiro M, Silveira JAG (2011) Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress. Plant Cell Environ 34: 1705-1722
11. Bonilla PJ, Dvorak DM, Deal K, Gregorio G (2002) RLFP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philipp J Agric Sci 85: 68-76
12. Chin JH, Lu X, Haefele SM, Gamuyao R, Ismail A, Wissuwa M, Heuer S (2009) Development and application of gene-based markers for the major rice QTL Phosphorus uptake 1. Theor Appl Genet 120: 1073-1086
13. Cooper NTW, Siebenmorgen TJ, Counce PA (2008) Effects of nighttime temperature during kernel development on rice physicochemical properties. Cereal Chem 85: 276-282
14. Cruz ND, Khush GS (2000) Rice grain quality evaluation procedures. In: Singh RK, Singh US, Khush GS (eds) Aromatic Rices. Oxford and IBH Publishing Co. Pvt. Ltd., New Delhi, pp 15-28
15. Dat JF, Foyer CH, Scott IM (1998a) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118: 1455-1461
16. 2 and catalase during thermo-tolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116: 1351-1357
17. Demiral T, Türkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53: 247-257
18. Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2, 6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci USA 92: 11312-11316
19. Fitzgerald MA, Resurreccion AP (2009) Maintaining the yield of edible rice in a warming world. Funct Plant Biol 36: 1037-1045
20. Fitzgerald MA, McCouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trends Plant Sci 14: 133-139
21. Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119: 355-364
22. Fukuoka M, Yoshimoto M, Hasegawa T (2012) MINCER: a novel instrument for monitoring the micrometeorology of rice canopies. J Agric Meteorol 68: 135-147
23. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488: 535-539
24. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48: 909-930
25. Guimaraes EP (2009) Rice breeding. In: Carena MJ (ed) Cereals. Handbook of Plant Breeding. Springer Science+Business Media, New York, USA, pp 99-126
26. Hasegawa T, Kuwagata T, Nishimori M, Ishigooka Y, Murakami M, Yoshimoto M, Kondo M, Ishimaru T, Sawan S, Masaki Y, Matsuzaki H (2009) Recent warming trends and rice growth and yield in Japan. MARCO Symposium on Crop Production under Heat Stress: Monitoring, Impact Assessment and Adaptation. Proceedings of the MARCO symposium, 5 to 9 October 2009, Tsukuba, Japan.
27. He Y, Huang B (2010) Differential responses to heat stress in activities and isozymes of four antioxidant enzymes for two cultivars of Kentucky bluegrass contrasting in heat tolerance. J Am Soc Hortic Sci 135: 116-124
28. IPCC (2013). Working Group I Contribution to the IPCC Fifth Assessment Report Climate Change 2013: The Physical Science Basis, Summary for Policymakers. http://www.climatechange2013.org/images/report/WG1AR5_SPM_FINAL.pdf; Accessed on October 27 2014.
29. Ishimaru T, Hirabayashi H, Ida M, Takai T, San-Oh YA, Yoshinaga S, Ando I, Ogawa T, Kondo M (2010) A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Ann Bot 106: 515-520
30. Jagadish SVK, Craufurd PQ, Wheeler TR (2008) Phenotyping rice mapping population parents for heat tolerance during anthesis. Crop Sci 48: 1140-1146
31. Jagadish SVK, Cairns J, Lafitte R, Wheeler TR, Price AH, Craufurd PQ (2010a) Genetic analysis of heat tolerance at anthesis in rice (Oryza sativa L.). Crop Sci 50: 1-9
32. Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010b) Physiological and proteomic approaches to dissect reproductive stage heat tolerance in rice (Oryza sativa L.). J Exp Bot 61: 143-156
33. Jagadish SVK, Muthurajan R, Rang ZW, Malo R, Heuer S, Bennett J, Craufurd PQ (2011) Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22). Rice 4: 1-11
34. Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53: 2401-2410
35. Julia C, Dingkuhn M (2013) Predicting temperature induced sterility of rice spikelets requires simulation of crop generated microclimate. Eur J Agron 49: 50-60
36. Juliano BO (1971) A simplified assay for milled rice amylase. Cereal Sci Today 16: 334-340
37. Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115: 571-576
38. Khush GS, Paule CM, de la Cruz NM (1979) Rice grain quality evaluation and improvement at IRRI. Proceedings of the Workshop on Chemical Aspects of Rice Grain Quality, International Rice Research Institute, Los Baños, Laguna, Philippines, pp 21-31
39. Kuk YI, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43: 2109-2117
40. Kumar A, Bernier J, Verulkar S, Lafitte HR, Atlin GN (2008) Breeding for drought tolerance: direct selection for yield, response to selection and use of drought-tolerant donors in upland and lowland-adapted populations. Field Crops Res 107: 221-231
41. Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161: 405-413
42. Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128: 682-695
43. Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138: 882-897
44. Li CY, Peng CH, Zhao QB, Xie P, Chen W (2004) Characteristic analysis of the abnormal high temperature in 2003's midsummer in Wuhan City. J Cen China Nor Univ Nat Sci 38: 379-381
45. Lin C, Li C, Lin S, Yang F, Huang J, Liu Y, Lur H (2010) Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in rice (Oryza sativa L.). J Agric Food Chem 58: 10545-10552
46. Lisle AJ, Martin M, Fitzgerald MA (2000) Chalky and translucent rice grains differ in starch composition and structure and cooking properties. Cereal Chem 77: 627-632
47. Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP, Naylor RL (2008) Prioritizing climate change adaptation needs for food security in 2030. Science 319: 607-610
48. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275
49. 2 and high temperature on seed-set and grain quality of rice. J Exp Bot 63: 3843-3852
50. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410
51. Mohammed AR, Tarpley L (2009) High nighttime temperatures affect rice productivity through altered pollen germination and spikelet fertility. Agric For Meteorol 149: 999-1008
52. Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99: 1161-1173
53. Mosse J (1990) Nitrogen-to-protein conversion factor for ten cereals and six legumes or oilseeds. A reappraisal of its definition and determination. Variation according to species and to seed protein content. J Agric Food Chem 38: 18-24
54. Nahakpam S, Shah K (2011) Expression of key antioxidant enzymes under combined effect of heat and cadmium toxicity in growing rice seedlings. Plant Growth Regul 63: 23-35
55. Neto ADA, Prisco JT, Eneas-Filho J, Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56: 87-94
56. 2 as an alternative electronic sink in photosynthesis? Curr Opin Plant Biol 5: 193-198
57. Prasad PVV, Boote KJ, Allen LH, Sheehy JE, Thomas JMG (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Res 95: 398-411
58. Rang ZW, Jagadish SVK, Zhou QM, Craufurd PQ, Heuer S (2011) Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environ Exp Bot 70: 58-65
59. Sairam RK, Srivastava GC, Saxena DC (2000) Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes. Biol Plant 43: 245-251
60. Sato Y, Murakami T, Funatsuki H, Matsuba S, Saruyama H, Tanida M (2001) Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings. J Exp Bot 52: 145-151
61. Selote DS, Chopra RK (2004) Drought-induced spikelet sterility is associated with an inefficient antioxidant defence in rice panicles. Physiol Plant 121: 462-471
62. Senthil-Kumar M, Kumar G, Srikanthbabu V, Udayakumar M (2007) Assessment of variability in acquired thermotolerance: potential option to study genotypic response and the relevance of stress genes. J Plant Physiol 164: 111-125
63. Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, Ismail AM, Mackill DJ (2009) Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Ann Bot 103: 151-160
64. Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167: 541-550
65. Sheehy JE, Mabilangan AE, Dionora MJA, Pablico PP (2007) Time of day of flowering in wild species of the genus Oryza. Int Rice Res Notes 32: 12-13
66. Shi W, Ishimaru T, Gannaban RB, Oane W, Jagadish SVK (2014) Popular rice (Oryza sativa L.) cultivars show contrasting responses to heat stress at gametogenesis and anthesis. Crop Sci. DOI: 10.2135/cropsci2014.01.0054
67. Sie M, Sanni K, Futakuchi K, Manneh B, Mande S, Vodouhe R, Dogbe S, Drame K, Ogunbayo A, Ndjiondjop M, Traore K (2012) Towards a rational use of African rice (Oryza glabrrima Steud.) for breeding in Sub-Saharan Africa. Genes Genomes Genomics 6: 1-7
68. Silva EN, Ferreira-Silva SL, Fontenele ADV, 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. J Plant Physiol 167: 1157-1164
69. Sung DY, Kaplan F, Lee KJ, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8: 179-187
70. Teixeira EI, Fischer G, van Velthuizen H, Walter C, Ewert F (2013) Global hot-spots of heat stress on agricultural crops due to climate change. Agric For Meteorol 170: 206-215
71. Venuprasad R, Lafitte HR, Atlin GN (2007) Response to direct selection for grain yield under drought stress in rice. Crop Sci 47: 285-293
72. Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162: 465-472
73. Wassmann R, Jagadish SVK, Sumfleth K, Pathak H, Howell G, Ismail A, Serraj R, Redona E, Singh RK, Heuer S (2009) Regional vulnerability of climate change impacts on Asian rice production and scope for adaptation. Adv Agron 102: 91-133
74. Weerakoon WMW, Maruyama A, Ohba K (2008) Impact of humidity on temperature-induced grain sterility in rice (Oryza sativa L). J Agron Crop Sci 194: 135-140
75. Welch JR, Vincent JR, Auffhammer M, Moya PF, Dobermann A, Dawe D (2010) Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures. Proc Natl Acad Sci USA 107: 14562-14567
76. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene response factor-like gene that confers submergence tolerance to rice. Nature 442: 705-708
77. Yang C, Heilman JL (1993) Responses of rice (Oryza sativa L.) to short term high temperature: growth development and yield. J Agric Res China 42: 1-11
78. Yang HC, Huang ZQ, Jiang ZY, Wang XW (2004) High temperature damage and its protective technologies of early and middle season rice in Anhui province. J Anhui Agric Sci 32: 3-4
79. Ye C, Argayoso MA, Redoña ED, Sierra SN, Laza MA, Dilla CJ, Mo Y, Thomson MJ, Chin J, Delaviña CB, Diaz GQ, Hernandez JE (2012) Mapping QTL for heat tolerance at flowering stage in rice using SNP markers. Plant Breed 131: 33-41
80. Yoshida S, Satake T, Mackill D (1981) High temperature stress. IRRI Res Paper Series 67: 1-15
81. Zou J, Liu AL, Chen XB, Zhou XY, Gao GF, Wang WF, Zhang XW (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166: 851-861