The metabolic basis of pollen thermo-tolerance: Perspectives for breeding

Metabolites

Volumn 4, Issue 4, 2014, Pages 889-920

  Paupière, Marine J ^a   van Heusden, Adriaan W ^a   Bovy, Arnaud G ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Breeding; Heat stress; High temperature; Metabolite; Pollen; Thermotolerance

Indexed keywords

EID: 85016474688     PISSN: None     EISSN: 22181989     Source Type: Journal    
DOI: 10.3390/metabo4040889     Document Type: Review

References (165)

1. Mittler, R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006, 11, 15-19.
2. Ainsworth, E.A.; Ort, D.R. How do we improve crop production in a warming world? Plant Physiol. 2010, 154, 526-530.
3. Wahid, A.; Gelani, S.; Ashraf, M.; Foolad, M. Heat tolerance in plants: An overview. Environ. Exp. Bot. 2007, 61, 199-223.
4. Intergovernmental Panel on Climate Change (IPCC). Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. In Special Report of the Intergovernmental Panel on Climate Change; Field, C.B., Barros, V., Stocker, T.F., Dahe, Q., Eds.; Cambridge University Press: Cambridge, UK, 2012; p. 582.
5. Hasanuzzaman, M.; Nahar, K.; Alam, M.M.; Roychowdhury, R.; Fujita, M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 2013, 14, 9643-9684.
6. Allakhverdiev, S.I.; Kreslavski, V.D.; Klimov, V.V.; Los, D.A.; Carpentier, R.; Mohanty, P. Heat stress: An overview of molecular responses in photosynthesis. Photosynth. Res. 2008, 98, 541-550.
7. Yamamoto, Y.; Aminaka, R.; Yoshioka, M.; Khatoon, M.; Komayama, K.; Takenaka, D.; Yamashita, A.; Nijo, N.; Inagawa, K.; Morita, N.; et al. Quality control of photosystem ii: Impact of light and heat stresses. Photosynth. Res. 2008, 98, 589-608.
8. Demirevska-Kepova, K.; Feller, U. Heat sensitivity of rubisco, rubisco activase and rubisco binding protein in higher plants. Acta Physiol. Plant. 2004, 26, 103-114.
9. Bokszczanin, K.L.; Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium; Fragkostefanakis, S. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front. Plant. Sci. 2013, doi:10.3389/fpls.2013.00315.
10. De Storme, N.; Geelen, D. The impact of environmental stress on male reproductive development in plants: Biological processes and molecular mechanisms. Plant Cell Environ. 2014, 37, 1-18.
11. Dane, F.; Hunter, A.G.; Chambliss, O.L. Fruit set, pollen fertility, and combining ability of selected tomato genotypes under high temperature field conditions. J. Am. Soc. Hort. Sci. 1991, 116, 906-910.
12. Firon, N.; Shaked, R.; Peet, M.M.; Pharr, D.M.; Zamski, E.; Rosenfeld, K.; Althan, L.; Pressman, E. Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci. Hort. 2006, 109, 212-217.
13. Frank, G.; Pressman, E.; Ophir, R.; Althan, L.; Shaked, R.; Freedman, M.; Shen, S.; Firon, N. Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ros scavengers, hormones, and sugars in the heat stress response. J. Exp. Bot. 2009, 60, 3891-3908.
14. Li, W.; Wei, Z.; Qiao, Z.; Wu, Z.; Cheng, L.; Wang, Y. Proteomics analysis of alfalfa response to heat stress. PloS One 2013, 8, e82725.
15. Kaplan, F.; Kopka, J.; Haskell, D.W.; Zhao, W.; Schiller, K.C.; Gatzke, N.; Sung, D.Y.; Guy, C.L. Exploring the temperature-stress metabolome of arabidopsis. Plant Physiol. 2004, 136, 4159-4168.
16. Liu, X.; Huang, B. Carbohydrate accumulation in relation to heat stress tolerance in two creeping bentgrass cultivars. J. Am. Soc. Hort. Sci. 2000, 125, 442-447.
17. Chaitanya, K.V.; Sundar, D.; Reddy, A.R. Mulberry leaf metabolism under high temperature stress. Biol. Plantarum 2001, 44, 379-384.
18. Rizhsky, L.; Liang, H.; Shuman, J.; Shulaev, V.; Davletova, S.; Mittler, R. When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004, 134, 1683-1696.
19. Al-Whaibi, M.H. Plant heat-shock proteins: A mini review. J. King Saud. Univ. Sci. 2011, 23, 139-150.
20. Kregel, K.C. Heat shock proteins: Modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. physiol. 2002, 92, 2177-2186.
21. Almeselmani, M.; Deshmukh, P.S.; Sairam, R.K.; Kushwaha, S.R.; Singh, T.P. Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 2006, 171, 382-388.
22. Hayat, S.; Hayat, Q.; Alyemeni, M.N.; Wani, A.S.; Pichtel, J.; Ahmad, A. Role of proline under changing environments: A review. Plant Signal Behav. 2012, 7, 1456-1466.
23. Chen, T.H.; Murata, N. Glycinebetaine protects plants against abiotic stress: Mechanisms and biotechnological applications. Plant Cell. Environ. 2011, 34, 1-20.
24. Kinnersley, A.M.; Turano, F.J. Gamma aminobutyric acid (gaba) and plant responses to stress. Crit. Rev. Plant Sci. 2000, 19, 479-509.
25. Strzalka, K.; Kostecka-Gugala, A.; Latowski, D. Carotenoids and environmental stress in plants: Significance of carotenoid-mediated modulation of membrane physical properties. Russ. J. Plant physiol. 2003, 50, 168-172.
26. Noctor, G.; Foyer, C.H. Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49, 249-279.
27. Caverzan, A.; Passaia, G.; Barcellos Rosa, S.; Werner Ribeiro, C.; Lazzarotto, F.; Margis-Pinheiro, M. Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 2012, 35, 1011-1019.
28. Twell, D. Plant reproduction, annual plant reviews. Pollen Developmental Biology; O'Neill, S.D., Roberts, J.A., Eds.; Sheffield Academic Press: Sheffield, UK, 2002; Volume 6.
29. Honys, D.; Renak, D.; Twell, D. Male Gametophyte Development and Function. Available online: http://www.ueb.cas.cz/cs/system/files/users/public/2006__Honys_Male_gametophyte__FOPB.pdf (accessed on 10 September 2014).
30. Pacini, E.; Jacquard, C.; Clement, C. Pollen vacuoles and their significance. Planta 2011, 234, 217-227.
31. Taylor, L.P. Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48, 461-491.
32. Sawhney, V.K.; Bhadula, S.K. Microsporogenesis in the normal and male-sterile stamenless-2 mutant of tomato (Lycopersicon esculentum). Can. J. Bot. 1988, 66, 2013-2021.
33. Pressman, E.; Peet, M.M.; Pharr, D.M. The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrates concentration in the developing anthers. Ann. Bot. 2002, 2002, 631-636.
34. Eveland, A.L.; Jackson, D.P. Sugars, signalling, and plant development. J. Exp. Bot. 2012, 63, 3367-3377.
35. Banga, S.S.; Labana, K.S.; Banga, S.K. Male sterility in indian mustard (Brassica juncea L. coss)-A biochemical characterization. Theor. Appl. Genet. 1984, 67, 515-519.
36. Pacini, E. Types and meaning of pollen carbohydrate reserves. Sex. Plant Reprod. 1996, 9, 362-366.
37. Roitsch, T. Source-sink regulation by sugar and stress. Plant Biol. 1999, 2, 198-206.
38. Koch, K. Sucrose metabolism: Regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 2004, 7, 235-246.
39. Singh, M.B.; Knox, R.B. Invertases of lilium pollen. Plant physiol. 1984, 74, 510-515.
40. Castro, A.J.; Clement, C. Sucrose and starch catabolism in the anther of lilium during its development: A comparative study among the anther wall, locular fluid and microspore/pollen fractions. Planta 2007, 225, 1573-1582.
41. Goetz, M.; Godt, D.E.; Guivarc'h, A.; Kahmann, U.; Chriqui, D.; Roitsch, T. Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc. Natl. Acad. Sci. USA 2001, 98, 6522-6527.
42. Le Roy, K.; Vergauwen, R.; Struyf, T.; Yuan, S.; Lammens, W.; Matrai, J.; de Maeyer, M.; van den Ende, W. Understanding the role of defective invertases in plants: Tobacco nin88 fails to degrade sucrose. Plant Physiol. 2013, 161, 1670-1681.
43. García, C.C.; Guarnieri, M.; Pacini, E. Inter-conversion of carbohydrate reserves from pollen maturation to rehydration in a chili pepper. Am. J. Plant Sci. 2013, 4, 1181-1186.
44. Clément, C.; Audran, J.-C. Anther wall layers control pollen sugar nutrition in Lilium. Protoplasma 1995, 187, 172-181.
45. Clement, C.; Burrus, M.; Audran, J.-C. Floral organ growth and carbohydrate content during pollen development in Lilium. Am. J. Bot. 1996, 83, 459-469.
46. Pressman, E.; Shaked, R.; Shen, S.; Altahan, L.; Firon, N. Variations in carbohydrate content and sucrose-metabolizing enzymes in tomato (Solanum lycopersicum L.) stamen parts during pollen maturation. Am. J. Plant Sci. 2012, 3, 252-260.
47. 2 fixation in the flower bud of Lilium. Ii. Anther. Int. J. Plant Sci. 1997, 158, 801-810.
48. Lehmann, S.; Funck, D.; Szabados, L.; Rentsch, D. Proline metabolism and transport in plant development. Amino Acids 2010, 39, 949-962.
49. Szabados, L.; Savoure, A. Proline: A multifunctional amino acid. Trends Plant Sci. 2009, 15, 89-97.
50. Mutters, R.G.; Ferreira, L.G.R.; Hall, A.E. Proline content of the anthers and pollen of heat-tolerant and heat-sensitive cowpea subjected to different temperatures. Crop Sci. 1989, 29, 1497-1500.
51. Sangwan, R.S. Change in the amino-acid content during male gametophyte formation of Datura metel in situ. Theor. Appl. Genet. 1978, 52, 221-225.
52. Mattioli, R.; Biancucci, M.; Lonoce, C.; Costantino, P.; Trovato, M. Proline is required for male gametophyte development in arabidopsis. BMC Plant Biol. 2012, doi:10.1186/1471-2229-12-236.
53. Edlund, A.F.; Swanson, R.; Preuss, D. Pollen and stigma structure and function: The role of diversity in pollination. Plant Cell 2004, 16, S84-S97.
54. Rodriguez-Garcia, M.I.; M'Rani-Alaoui, M.; Fernandez, M.C. Behavior of storage lipids during development and germination of olive (Olea europaea L.) pollen. Protoplasma 2003, 221, 237-244.
55. Tütüncü, K.S.; Dane, F.; Tütüncü, S. Distribution of insoluble polysaccharides, neutral lipids, and proteins in the developing anthers of Campsis radicans (L.) seem. (bignoniaceae). Plant Syst. Evol. 2013, 299, 743-760.
56. Wolters-Arts, M.; Lush, W.M.; Mariani, C. Lipids are required for directional pollen-tube growth. Nature 1998, 392, 818-821.
57. May, M.J.; Vernoux, T.; Leaver, C.; van Montagu, M.; Inzé, D. Glutathione homeostasis in plants: Implications for environmental sensing and plant development. J. Exp. Bot. 1998, 49, 649-667.
58. Szalai, G.; Kellős, T.; Galiba, G.; Kocsy, G. Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J. Plant Growth Regul. 2009, 28, 66-80.
59. Zechmann, B.; Koffler, B.E.; Russell, S.D. Glutathione synthesis is essential for pollen germination in vitro. BMC Plant Biol. 2011, doi:10.1186/1471-2229-11-54.
60. Agati, G.; Azzarello, E.; Pollastri, S.; Tattini, M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 2012, 196, 67-76.
61. Brunetti, C.; Di Ferdinando, M.; Fini, A.; Pollastri, S.; Tattini, M. Flavonoids as antioxidants and developmental regulators: Relative significance in plants and humans. Int. J. Mol. Sci. 2013, 14, 3540-3555.
62. Ylstra, B.; Touraev, A.; Moreno, R.M.B.; Stoger, E.; Tunen Van, A.J.; Vicente, O.; Mol, J.N.M.; Heberle-Bors, E. Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol. 1992, 100, 902-907.
63. Mo, Y.; Nagel, C.; Taylor, L.P. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl. Acad. Sci. 1992, 89, 7213-7217.
64. Napoli, C.A.; Fahy, D.; Wang, H.-Y.; Taylor, L.P. White anther: A petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol. 1999, 120, 615-622.
65. Schijlen, E.G.; de Vos, C.H.; Martens, S.; Jonker, H.H.; Rosin, F.M.; Molthoff, J.W.; Tikunov, Y.M.; Angenent, G.C.; van Tunen, A.J.; Bovy, A.G. Rna interference silencing of chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiol. 2007, 144, 1520-1530.
66. Burbulis, I.E.; Iacobucci, V.; Shirley, B.W. A null mutation in the first enzyme of flavonoid biosynthesis does not affect male fertility in arabidopsis. Plant Cell 1996, 8, 1013-1025.
67. Evans, P.T.; Malmberg, R.L. Do polyamines have roles in plant development? Annu. Rev. Plant Physiol. Plant Mol. Biol. 1989, 40, 235-269.
68. Chibi, F.; Angosto, T.; Garrido, D.; Matilla, A. Requirement of polyamines for in vitro maturation of the mid-binucleate pollen of Nicotiana Tabacum. J. Plant Physiol. 1993, 142, 452-456.
69. Song, J.; Nada, K.; Tachibana, S. The early increase of s-adenosylmethionine decarboxylase activity is essential for the normal germination and tube growth in tomato (Lycopersicon esculentum mill.) pollen. Plant Sci. 2001, 161, 507-515.
70. Falasca, G.; Franceschetti, M.; Bagni, N.; Altamura, M.M.; Biasi, R. Polyamine biosynthesis and control of the development of functional pollen in kiwifruit. Plant Physiol. Biochem. 2010, 48, 565-573.
71. Parish, R.W.; Phan, H.A.; Iacuone, S.; Li, S.F. Tapetal development and abiotic stress: A centre of vulnerability. Funct. Plant Biol. 2013, 39, 553-559.
72. Ellis, C.M.; Nagpal, P.; Young, J.C.; Hagen, G.; Guilfoyle, T.J.; Reed, J.W. Auxin response factor1 and auxin response factor2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 2005, 132, 4563-4574.
73. De Jong, M.; Mariani, C.; Vriezen, W.H. The role of auxin and gibberellin in tomato fruit set. J. Exp. Bot. 2009, 60, 1523-1532.
74. Abeles, F.B.; Rubinstein, B. Regulation of ethylene evolution and leaf abscission by auxin. Plant Physiol. 1963, 39, 963-969.
75. Tanaka, M.; Takei, K.; Kojima, M.; Sakakibara, H.; Mori, H. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J. 2006, 45, 1028-1036.
76. Mano, Y.; Nemoto, K. The pathway of auxin biosynthesis in plants. J. Exp. Bot. 2012, 63, 2853-2872.
77. Cheng, Y.; Dai, X.; Zhao, Y. Auxin biosynthesis by the yucca flavin monooxygenases controls the formation of floral organs and vascular tissues in arabidopsis. Genes Dev. 2006, 20, 1790-1799.
78. Cecchetti, V.; Altamura, M.M.; Falasca, G.; Costantino, P.; Cardarelli, M. Auxin regulates arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 2008, 20, 1760-1774.
79. Cecchetti, V.; Altamura, M.M.; Brunetti, P.; Petrocelli, V.; Falasca, G.; Ljung, K.; Costantino, P.; Cardarelli, M. Auxin controls arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. Plant J. 2013, 74, 411-422.
80. Yang, H.; Wei, Z.; Xu, Z. Effects of specific expression of iaal gene in tobacco tapetum on pollen embryogenesis. Sci. China 1997, 40, 384-391.
81. Daviere, J.M.; Achard, P. Gibberellin signaling in plants. Development 2013, 140, 1147-1151.
82. Goto, N.; Pharis, R.P. Role of gibberellins in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana. Can. J. Bot. 1999, 77, 944-954.
83. Chhun, T.; Aya, K.; Asano, K.; Yamamoto, E.; Morinaka, Y.; Watanabe, M.; Kitano, H.; Ashikari, M.; Matsuoka, M.; Ueguchi-Tanaka, M. Gibberellin regulates pollen viability and pollen tube growth in rice. Plant Cell 2007, 19, 3876-3888.
84. Creelman, R.A.; Mullet, J.E. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48, 355-381.
85. McConn, M.; Browse, J. The critical requirement for linolenic acid, is pollen development, not photosynthesis, in an arabidopsis mutant. Plant Cell 1996, 8, 403-416.
86. Ishiguro, S.; Kawai-Oda, A.; Ueda, J.; Nishida, I.; Okada, K. The defective in anther dehiscence1 gene encodes a novel phospholipase a1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in arabidopsis. Plant Cell 2001, 13, 2191-2209.
87. De la Torre, F.; María del Carmen, R.-G.; Matilla, A.J. How ethylene works in the reproductive organs of higher plants. Plant Signal. Behav. 2006, 1, 231-242.
88. Kovaleva, L.V.; Dobrovolskaya, A.; Voronkov, A.; Rakitin, V. Ethylene is involved in the control of male gametophyte development and germination in petunia. J. Plant Growth Regul. 2010, 30, 64-73.
89. Rieu, I.; Wolters-Arts, M.; Derksen, J.; Mariani, C.; Weterings, K. Ethylene regulates the timing of anther dehiscence in tobacco. Planta 2003, 217, 131-137.
90. Xiong, L. Regulation of abscisic acid biosynthesis. Plant Physiol. 2003, 133, 29-36.
91. Frascaroli, E.; Tuberosa, R. Effect of abscisic acid on pollen germination and tube growth of maize genotypes. Plant Breed. 1993, 110, 250-254.
92. Yang, H.-Q.; Jie, Y.-L.; Liu, L.-X.; Tang, W.-Y.; Yu, M.-G. Regulation of abscisic acid and its biosynthesis inhibitors on pomegranate pollen germination and tube growth. Acta Hort. 2003, 620, 209-213.
93. Fridman, Y.; Savaldi-Goldstein, S. Brassinosteroids in growth control: How, when and where. Plant Sci. 2013, 209, 24-31.
94. Ariizumi, T.; Kawanabe, T.; Hatakeyama, K.; Sato, S.; Kato, T.; Tabata, S.; Toriyama, K. Ultrastructural characterization of exine development of the transient defective exine 1 mutant suggests the existence of a factor involved in constructing reticulate exine architecture from sporopollenin aggregates. Plant Cell Physiol. 2008, 49, 58-67.
95. Saini, H.S.; Sedgley, M.; Aspinall, D. Developmental anatomy in wheat of male sterility induced by heat stress, water deficit or abscissic acid. Aust. J. Plant Physiol. 1984, 11, 243-253.
96. Abdul-Baki, A.A.; Stommel, J.R. Pollen viability and fruit set of tomato genotypes under optimum and high-temperature regimes. HortScience 1995, 30, 115-117.
97. Ploeg Van der, A.; Heuvelink, E. Influence of sub-optimal temperature on tomato growth and yield: A review. J. Hortic. Sci. Biotech. 2005, 80, 652-659.
98. Hurd, R.G.; Cooper, A.J. The effect of early low temperature treatment on the yield of single inflorescence tomatoes. J. Hortic. Sci. 1970, 45, 19-27.
99. Peet, M.M.; Sato, S.; Gardner, R.G. Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant Cell Environ. 1998, 21, 225-231.
100. Sato, S.; Kamiyama, M.; Iwata, T.; Makita, N.; Furukawa, H.; Ikeda, H. Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann. Bot. 2006, 97, 731-738.
101. Sakata, T.; Takahashi, H.; Nishiyama, I.; Higashitani, A. Effects of high temperature on the development of pollen mother cells and microspores in barley Hordeum vulgare L. J. Plant Res. 2000, 113, 395-402.
102. Prasad, P.V.V.; Boote, K.J.; Allen, L.H.; Sheehy, J.E.; Thomas, J.M.G. Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crop. Res. 2006, 95, 398-411.
103. Matsui, T.; Omasa, K. Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: Anther characteristics. Ann. Bot. 2002, 89, 683-687.
104. Devasirvatham, V.; Gaur, P.M.; Mallikarjuna, N.; Tokachichu, R.N.; Trethowan, R.M.; Tan, D.K.Y. Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments. Funct. Plant Biol. 2012, 39, 1009-1018.
105. Herrero, M.P.; Johnson, R.R. High temperature stress and pollen viability of maize. Crop Sci. 1980, 20, 796-800.
106. Kim, S.Y.; Hong, C.B.; Lee, I. Heat shock stress causes stage-specific male sterility in Arabidopsis thaliana. J. Plant Res. 2001, 114, 301-307.
107. Young, L.W.; Wilen, R.W.; Bonham-Smith, P.C. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. J. Exp. Bot. 2004, 55, 485-495.
108. Harsant, J.; Pavlovic, L.; Chiu, G.; Sultmanis, S.; Sage, T.L. High temperature stress and its effect on pollen development and morphological components of harvest index in the c3 model grass Brachypodium distachyon. J. Exp. Bot. 2013, 64, 2971-2983.
109. Porch, T.G.; Jahn, M. Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris. Plant Cell Environ. 2001, 24, 723-731.
110. Prasad, P.V.; Craufurd; Summerfield, R.J. Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress. Ann. Bot. 1999, 84, 381-386.
111. Aloni, B.; Peet, M.; Pharr, M.; Karni, L. The effect of high temperature and high atmospheric co2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. Physiol. Plant. 2001, 112, 505-512.
112. Djanaguiraman, M.; Prasad, P.V.V.; Boyle, D.L.; Schapaugh, W.T. Soybean pollen anatomy, viability and pod set under high temperature stress. J. Agron. Crop. Sci. 2013, 199, 171-177.
113. Kaushal, N.; Awasthi, R.; Gupta, K.; Gaur, P.; Siddique, K.H.M.; Nayyar, H. Heat-stress-induced reproductive failurs in chikpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Funct. Plant Biol. 2013, 40, 1334-1349.
114. Ledesma, N.; Sugiyama, N. Pollen quality and pperformance in strawberry plants exposed to high-temperature stress. J. Amer. Soc. Hort. Sci 2005, 130, 341-347.
115. Iwahori, S. High temperature injuries in tomato. IV. Development of normal flower buds and morphological abnormalities of flower buds treated with high temperature. J. Jpn. Soc. Hort. Sci. 1965, 35, 55-62.
116. Sato, S.; M.M., P.; Thomas, J.F. Determining critical pre- and post-anthesis periods and physiological processes in Lycopersicon esculentum mill. Exposed to moderatly elevated temperatures. J. Exp. Bot. 2002, 53, 1187-1195.
117. Ahmed, F.E.; Hall, A.E.; DeMason, D.A. Heat injury during floral development in cowpea (Vigna unguiculata, fabaceae). Am. J. Bot. 1992, 79, 784-791.
118. Prasad, P.V.; Craufurd, P.Q.; Kakani, V.G.; Wheeler, T.R.; Boote, K.J. Influence of high temperature during pre- and post-anthesis stages of floral development on fruit-set and pollen germination in peanut. Aust. J. Plant Physiol 2001, 28, 233-240.
119. Erickson, A.N.; Markhart, A.H. Flower developmental stage and organ sensitivity of bell pepper (Capsicum annum l.) to elevated temperature. Plant Cell Environ. 2002, 25, 123-130.
120. Oshino, T.; Abiko, M.; Saito, R.; Ichiishi, E.; Endo, M.; Kawagishi-Kobayashi, M.; Higashitani, A. Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol. Genet. Genomics 2007, 278, 31-42.
121. Suzuki, K.; Takeda, H.; Tsukaguchi, T.; Egawa, Y. Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress. Sex. Plant Reprod. 2001, 13, 293-299.
122. Hazra, P.; Ansary, S.H. Genetics of heat tolerance for floral and fruit set to high temperature stress in tomato (Lycopersicon esculentum mill.). Sabrao J. breed. Genet. 2008, 40, 117-125.
123. Kakani, V.G.; Reddy, K.R.; Koti, S.; Wallace, T.P.; Prasad, P.V.; Reddy, V.R.; Zhao, D. Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Ann. Bot. 2005, 96, 59-67.
124. Vasil, I.K. Developing cell and tissue culture systems for the improvement of cereals and grass crops. J. Plant Physiol. 1987, 128, 193-218.
125. Johannsson, M.H.; Stephenson, A.G. Effects of temperature during microsporogenesis on pollen performance in Cucurbita pepo L. (cucurbitaceae). Int. J. Plant Sci. 1998, 159, 616-626.
126. Sato, S.; Peet, M.M.; Thomas, J.F. Physiological factors limit fruit set of tomato (Lycopersicon esculentum mill.) under chronic, mild heat stress. Plant Cell Environ. 2000, 23, 719-726.
127. Sato, S.; Peet, M.M.; Gardner, R.G. Formation of parthenocarpic fruit, undeveloped flowers and aborted flowers in tomato under moderately elevated temperatures. Sci. Hort. 2001, 90, 243-254.
128. Abdelmageed, A.; Gruda, N. Influence of high temperatures on gas exchange rate and growth of eight tomato cultivars under controlled heat stress conditions. Europ. J. Hort. Sci. 2009, 74, 152-159.
129. Li, Z.; Palmer, W.M.; Martin, A.P.; Wang, R.; Rainsford, F.; Jin, Y.; Patrick, J.W.; Yang, Y.; Ruan, Y.-L. High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into and heat tolerance of young fruit. J. Exp. Bot. 2011, 63, 1155-1166.
130. Jain, M.; Prasad, P.V.; Boote, K.J.; Hartwell, A.L., Jr.; Chourey, P.S. Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor l. Moench). Planta 2007, 227, 67-79.
131. 2 enrichment. Ann. Bot. 2002, 90, 607-612.
132. Hong-Qi, Z.; Croes, A.F. Protection of pollen germination from adverse temperature: A possible role for proline. Plant Cell Environ. 1983, 6, 471-476.
133. Tang, R.-S.; Zheng, J.-C.; Jin, Z.-Q.; Zhang, D.-D.; Huang, Y.-H.; Chen, L.-G. Possible correlation between high temperature-induced floret sterility and endogenous levels of iaa, gas and aba in rice (Oryza sativa L.). Plant Growth Regul. 2008, 54, 37-43.
134. Prasad, P.V.V.; Djanaguiraman, M. High night temperature decreases leaf photosynthesis and pollen function in grain sorghum. Funct. Plant Biol. 2011, 38, 993-1003.
135. Fariduddin, Q.; Varshney, P.; Yusuf, M.; Ahmad, A. Polyamines: Potent modulators of plant responses to stress. J. Plant Interact. 2013, 8, 1-16.
136. Gupta, K.; Dey, A.; Gupta, B. Plant polyamines in abiotic stress responses. Acta Physiol. Plant. 2013, 35, 2015-2036.
137. Alcazar, R.; Marco, F.; Cuevas, J.C.; Patron, M.; Ferrando, A.; Carrasco, P.; Tiburcio, A.F.; Altabella, T. Involvement of polyamines in plant response to abiotic stress. Biotechnol. Lett. 2006, 28, 1867-1876.
138. Song, J.; Nada, K.; Tachibana, S. Ameliorative effect of polyamines on the high temperature inhibition of in vitro pollen germination in tomato (Lycopersicon esculentum mill.). Sci. Hort. 1999, 80, 203-212.
139. Song, J.; Nada, K.; Tachibana, S. Suppresion of s-adenosylmethionine decarboxylase activity is a major cause for high-temperature inhibition of pollen germination and tube growth in tomato (Lycopersicon esculentum mill.). Plant Cell Physiol. 2002, 43, 619-627.
140. Wolukau, J.N.; Zhang, S.; Xu, G.; Chen, D. The effect of temperature, polyamines and polyamine synthesis inhibitor on in vitro pollen germination and pollen tube growth of Prunus mume. Sci. Hort. 2004, 99, 289-299.
141. Mazorra, L.M. Brassinosteroid action and its relation with heat stress mechanisms in plants. In Brassinosteroids: A Class of Plant Hormone; Hayat, S., Ahmad, A., Eds.; Springer: New York, NY, USA, 2011; pp. 289-307.
142. Singh, I.; Shono, M. Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul. 2005, 47, 111-119.
143. Larkindale, J.; Knight, M.R. Protection against heat stress-induced oxidative damage in arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 2002, 128, 682-695.
144. Firon, N.; Pressman, E.; Meir, S.; Khoury, R.; Altahan, L. Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants 2012, doi:10.1093/aobpla/pls024.
145. Zhang, S.W.; Li, C.H.; Cao, J.; Zhang, Y.C.; Zhang, S.Q.; Xia, Y.F.; Sun, D.Y.; Sun, Y. Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by tld1/osgh3.13 activation. Plant Physiol. 2009, 151, 1889-1901.
146. Jain, M.; Khurana, J.P. Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J. 2009, 276, 3148-3162.
147. Sakata, T.; Oshino, T.; Miura, S.; Tomabechi, M.; Tsunaga, Y.; Higashitani, N.; Miyazawa, Y.; Takahashi, H.; Watanabe, M.; Higashitani, A. Auxins reverse plant male sterility caused by high temperatures. Proc. Natl. Acad. Sci. USA 2010, 107, 8569-8574.
148. Rudich, J.; Zamski, E.; Regev, Y. Genotypic variation for sensitivity to high temperature in the tomato: Pollination and fruit set. Bot. Gaz. 2013, 138, 448-452.
149. Nyquist, W.E.; Baker, R.J. Estimation of heritability and prediction of selection response in plant populations. Crit. Rev. Plant Sci. 1991, 10, 235-322.
150. Acquaah, G. Principles of Plant Genetics and Breeding, 1st ed.; Blackwell Publishing: Hoboken, NJ, USA, 2007.
151. Hanson, P.M.; Chen, J.-T.; Kuo, G. Gene action and heritability of high-temperature fruit set in tomato line cl5915. HortScience 2002, 37, 172-175.
152. Hazra, P.; Ansary, S.H.; Dutta, A.K.; Balacheva, E.; Atanassova, B. Breeding tomato tolerant to high temperature stress. Acta Hort. 2009, 830, 241-248.
153. Jain, S.M., Brar, D.S., Eds. Molecular Techniques in Crop Improvement, 2nd ed.; Springer: New York, NY, USA, 2009.
154. Sadat, S.; Saeid, K.A.; Bihamta, M.R.; Torabi, S.; Salekdeh, S.G.H.; Ayeneh, G.A.L. Marker assisted selection for heat tolerance in bread wheat. J. World Appl. Sci. 2013, 21, 1181-1189.
155. Frova, C.; Sari-Gorla, M. Quantitative trait loci (QTLs) for pollen thermotolerance detected in maize. Mol. Gen. Genet. 1994, 245, 424-430.
156. Xiao, Y.-H.; Pan, Y.; Luo, L.-H.; Deng, H.-B.; Zhang, G.-L.; Tang, W.-B.; Chen, L.-Y. Quantitative trait loci associated with pollen fertility under high temperature stress at flowering stage in rice (Oryza sativa). Rice Sci. 2011, 18, 204-209.
157. Kardivel, P. Molecular breeding in vegetable crops-challenges and opportunities. In Proceeding of 2nd National Workshop on Marker-Assisted Selection for Crop Improvement, ICRISAT, Patancheru, India, 27-29 October 2010.
158. Grilli, G.V.G.; Braz, L.T.; Lemos, E.G.M. QTL identification for tolerance to fruit set in tomato by faflp markers. Crop Breed. Appl. Biotechnol. 2007, 7, 234-241.
159. Lin, K.-H.; Yeh, W.-L.; Chen, H.-M.; Lo, H.-F. Quantitative trait loci influencing fruit-related characteristics of tomato grown in high-temperature conditions. Euphytica 2010, 174, 119-135.
160. Ye, C.; Argayoso, M.A.; Redoña, E.D.; Sierra, S.N.; Laza, M.A.; Dilla, C.J.; Mo, Y.; Thomson, M.J.; Chin, J.; Delaviña, C.B.; et al. Mapping qtl for heat tolerance at flowering stage in rice using snp markers. Plant Breed. 2012, 131, 33-41.
161. Jagadish, S.V.K.; Cairns, J.; Lafitte, R.; Wheeler, T.R.; Price, A.H.; Craufurd, P.Q. Genetic analysis of heat tolerance at anthesis in rice. Crop Sci. 2010, 50, 1633-1641.
162. Lucas, M.R.; Ehlers, J.D.; Huynh, B.-L.; Diop, N.-N.; Roberts, P.A.; Close, T.J. Markers for breeding heat-tolerant cowpea. Mol. Breed. 2012, 31, 529-536.
163. Colbert, T.; Till, B.J.; Tompa, R.; Reynolds, S.; Steine, M.N.; Yeung, A.T.; McCallum, C.M.; Comai, L.; Henikoff, S. High-throughput screening for induced point mutations. Plant Physiol. 2001, 126, 480-484.
164. Arbona, V.; Manzi, M.; Ollas, C.; Gomez-Cadenas, A. Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int. J. Mol. Sci. 2013, 14, 4885-4911.
165. Fernie, A.R.; Schauer, N. Metabolomics-assisted breeding: A viable option for crop improvement? Trends Genet. 2009, 25, 39-48.