Pollen development at high temperature: From acclimation to collapse

Plant Physiology

Volumn 173, Issue 4, 2017, Pages 1967-1976

  Rieu, Ivo ^a   Twell, David ^b   Firon, Nurit ^c  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACCLIMATIZATION; GROWTH, DEVELOPMENT AND AGING; HEAT; PHYSIOLOGY; POLLEN;

ACCLIMATIZATION; HOT TEMPERATURE; POLLEN;

EID: 85016492951     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.01644     Document Type: Article

References (103)

1. Abiko M, Akibayashi K, Sakata T, Kimura M, Kihara M, Itoh K, Asamizu E, Sato S, Takahashi H, Higashitani A (2005) High-temperature induction of male sterility during barley (Hordeum vulgare L.) anther development is mediated by transcriptional inhibition. Sex Plant Reprod 18: 91-100.
2. Ahmed FE, Hall AE, Demason DA (1992) Heat injury during floral development in cowpea (Vigna unguiculata, Fabaceae). Am J Bot 79: 784-791
3. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21: 1453-1472.
4. Bailey-Serres J (2013) Microgenomics: genome-scale, cell-specific monitoring of multiple gene regulation tiers. Annu Rev Plant Biol 64: 293-325.
5. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65: 1229-1240.
6. Bita CE, Zenoni S, Vriezen WH, Mariani C, Pezzotti M, Gerats T (2011) Temperature stress differentially modulates transcription in meiotic anthers of heat-tolerant and heat-sensitive tomato plants. BMC Genomics 12: 384
7. Bokszczanin KL, Fragkostefanakis S; Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci 4: 315
8. Burke JJ, Chen J (2015) Enhancement of reproductive heat tolerance in plants. PLoS One 10: e0122933
9. Carrizo García C, Nepi M, Pacini E (2017) It is a matter of timing: asynchrony during pollen development and its consequences on pollen performance in angiosperms-a review. Protoplasma 254: 57-73.
10. Chaturvedi P, Doerfler H, Jegadeesan S, Ghatak A, Pressman E, Castillejo MA, Wienkoop S, Egelhofer V, Firon N, Weckwerth W (2015) Heat treatment-responsive proteins in different developmental stages of tomato pollen detected by targeted mass accuracy precursor alignment (tMAPA). J Proteome Res 14: 4463-4471.
11. Chaturvedi P, Ischebeck T, Egelhofer V, Lichtscheidl I, Weckwerth W (2013) Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. J Proteome Res 12: 4892-4903.
12. Chen S, Liu A, Zhang S, Li C, Chang R, Liu D, Ahammed GJ, Lin X (2013) Overexpression of mitochondrial uncoupling protein conferred resistance to heat stress and Botrytis cinerea infection in tomato. Plant Physiol Biochem 73: 245-253.
13. Das P, Nutan KK, Singla-Pareek SL, Pareek A (2015) Understanding salinity responses and adopting ‘omics-based’ approaches to generate salinity tolerant cultivars of rice. Front Plant Sci 6: 712
14. Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108: 7247-7252.
15. Deng Y, Srivastava R, Quilichini TD, Dong H, Bao Y, Horner HT, Howell SH (2016) IRE1, a component of the unfolded protein response signaling pathway, protects pollen development in Arabidopsis from heat stress. Plant J 88: 193-204.
16. De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ 37: 1-18.
17. Djanaguiraman M, Prasad PVV, Boyle DL, Schapaugh WT (2013) Soybean pollen anatomy, viability and pod set under high temperature stress. J Agron Crop Sci 199: 171-177.
18. Djanaguiraman M, Prasad PVV, Murugan M, Perumal R, Reddy UK (2014) Physiological differences among sorghum (Sorghum bicolor L. Moench) genotypes under high temperature stress. Environ Exp Bot 100: 43-54.
19. Doukhanina EV, Chen S, van der Zalm E, Godzik A, Reed J, Dickman MB (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 281: 18793-18801.
20. Driedonks N, Xu J, Peters JL, Park S, Rieu I (2015) Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. Front Plant Sci 6: 999
21. Dupuis I, Dumas C (1990) Influence of temperature stress on in vitro fertilization and heat shock protein synthesis in maize (Zea mays L.) reproductive tissues. Plant Physiol 94: 665-670.
22. Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol 50: 1911-1922.
23. Fahad S, Hussain S, Saud S, Khan F, Hassan S, Amanullah, Nasim W, Arif M, Wang F, Huang J (2016) Exogenously applied plant growth regulators affect heat-stressed rice pollens. J Agron Crop Sci 202: 139-150.
24. Fessenden M (2016) Metabolomics: Small molecules, single cells. Nature 540: 153-155.
25. Firon N, Pressman E, Meir S, Khoury R, Altahan L (2012) Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants 2012: pls024
26. Firon N, Shaked R, Peet MM, Pharr DM, Zamski E, Rosenfeld K, Althan L, Pressman E (2006) Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci Hortic (Amsterdam) 109: 212-217.
27. Fragkostefanakis S, Mesihovic A, Hu Y, Schleiff E (2016a) Unfolded protein response in pollen development and heat stress tolerance. Plant Reprod 29: 81-91.
28. Fragkostefanakis S, Mesihovic A, Simm S, Paupière MJ, Hu Y, Paul P, Mishra SK, Tschiersch B, Theres K, Bovy A, Schleiff E, Scharf KD (2016b) HsfA2 controls the activity of developmentally and stressregulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol 170: 2461-2477.
29. Fragkostefanakis S, Simm S, Paul P, Bublak D, Scharf KD, Schleiff E (2015) Chaperone network composition in Solanum lycopersicum explored by transcriptome profiling and microarray meta-analysis. Plant Cell Environ 38: 693-709.
30. Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) 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 60: 3891-3908.
31. Frova C, Taramino G, Binelli G (1989) Heat-shock proteins during pollen development in maize. Dev Genet 10: 324-332.
32. Frova C, Taramino G, Ottaviano E (1991) Sporophytic and gametophytic heat shock protein synthesis in Sorghum bicolor. Plant Sci 73: 35-44.
33. Gagliardi D, Breton C, Chaboud A, Vergne P, Dumas C (1995) Expression of heat shock factor and heat shock protein 70 genes during maize pollen development. Plant Mol Biol 29: 841-856.
34. Giorno F, Wolters-Arts M, Grillo S, Scharf KD, Vriezen WH, Mariani C (2010) Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. J Exp Bot 61: 453-462.
35. Goetz M, Godt DE, Guivarc’h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98: 6522-6527.
36. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5: 1217-1229.
37. Gross Y, Kigel J (1994) Differential sensitivity to high temperature of stages in the reproductive development of common bean (Phaseolus vulgaris L.). Field Crops Res 36: 201-212.
38. Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol 103: 1067-1073.
39. Harsant J, Pavlovic L, Chiu G, Sultmanis S, Sage TL (2013) 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 64: 2971-2983.
40. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332.
41. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5: R85
42. Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64: 477-499.
43. Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23: 515-533.
44. Iwahori S (1965) High temperature injuries in tomato. IV. Development of normal flower buds and morphological abnormalities of flower buds treated with high temperature. J Jpn Soc Hortic Sci 34: 33-41.
45. Jacobsen SE, Olszewski NE (1991) Characterization of the arrest in anther development associated with gibberellin deficiency of the gib-1 mutant of tomato. Plant Physiol 97: 409-414.
46. Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61: 143-156.
47. Jain M, Prasad PVV, Boote KJ, Hartwell AL, Jr., Chourey PS (2007) Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor L. Moench). Planta 227: 67-79.
48. Kaur R, Bains TS, Bindumadhava H, Nayyar H (2015) Responses of mungbean (Vigna radiata L.) genotypes to heat stress: Effects on reproductive biology, leaf function and yield traits. Sci Hortic (Amsterdam) 197: 527-541.
49. Kim SY, Hong CB, Lee I (2001) Heat shock stress causes stage-specific male sterility in Arabidopsis thaliana. J Plant Res 114: 301-307.
50. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19: 479-509.
51. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63: 1593-1608
52. Kumar RR, Goswami S, Gadpayle KA, Singh K, Sharma SK, Singh GP, Pathak H, Rai RD (2014) Ascorbic acid at pre-anthesis modulate the thermotolerance level of wheat (Triticum aestivum) pollen under heat stress. J Plant Biochem Biotechnol 23: 293-306.
53. Lansac AR, Sullivan CY, Johnson BE (1996) Accumulation of free proline in sorghum (Sorghum bicolor) pollen. Can J Bot 74: 40-45.
54. Larkindale J, Huang BR (2005) Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul 47: 17-28.
55. Lee S-LJ, Warmke HE (1979) Organelle size and number in fertile and T-cytoplasmic male-sterile corn. Am J Bot 66: 141-148.
56. Li X, Lawas LMF, Malo R, Glaubitz U, Erban A, Mauleon R, Heuer S, Zuther E, Kopka J, Hincha DK, Jagadish KSV (2015) Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant Cell Environ 38: 2171-2192.
57. Luo D, et al (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45: 573-577.
58. Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: response to high temperature stress. J Photochem Photobiol B 137: 116-126.
59. McCormick S (2004) Control of male gametophyte development. Plant Cell (Suppl) 16: S142-S153
60. McLoughlin F, Basha E, Fowler ME, Kim M, Bordowitz J, Katiyar-Agarwal S, Vierling E (2016) Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress. Plant Physiol 172: 1221-1236.
61. Mesihovic A, Iannacone R, Firon N, Fragkostefanakis S (2016) Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reprod 29: 93-105.
62. Min L, Li Y, Hu Q, Zhu L, Gao W, Wu Y, Ding Y, Liu S, Yang X, Zhang X (2014) Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiol 164: 1293-1308.
63. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37: 118-125.
64. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498.
65. Müller F, Rieu I (2016) Acclimation to high temperature during pollen development. Plant Reprod 29: 107-118.
66. Müller F, Xu J, Kristensen L, Wolters-Arts M, de Groot PFM, Jansma SY, Mariani C, Park S, Rieu I (2016) High-temperature-induced defects in tomato (Solanum lycopersicum) anther and pollen development are associated with reduced expression of B-class floral patterning genes. PLoS One 11: e0167614
67. Mutters RG, Ferreira LGR, Hall AE (1989) Proline content of the anthers and pollen of heat-tolerant and heat-sensitive cowpea subjected to different temperatures. Crop Sci 29: 1497-1500.
68. Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22: 53-65.
69. Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A (2007) Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genomics 278: 31-42.
70. Pachauri RK, Allen MR, Barros VR, Broome J, Cramer W, Christ R, Church JA, Clarke L, Dahe Q, Dasgupta P, et al (2014) Climate Change 2014. Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland
71. Pacini E, Guarnieri M, Nepi M (2006) Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma 228: 73-77.
72. Parish RW, Li SF (2010) Death of a tapetum: A programme of developmental altruism. Plant Sci 178: 73-89.
73. Parish RW, Phan HA, Iacuone S, Li SF (2012) Tapetal development and abiotic stress: a centre of vulnerability. Funct Plant Biol 39: 553-559.
74. Peet MM, Sato S, Gardner RG (1998) Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant Cell Environ 21: 225-231.
75. Prasad PVV, Djanaguiraman M (2011) High night temperature decreases leaf photosynthesis and pollen function in grain sorghum. Funct Plant Biol 38: 993-1003.
76. Pressman E, Harel D, Zamski E, Shaked R, Althan L, Rosenfeld K, Firon N (2006) The effect of high temperatures on the expression and activity of sucrose-cleaving enzymes during tomato (Lycopersicon esculentum) anther development. J Hortic Sci Biotechnol 81: 341-348.
77. Pressman E, Peet MM, Pharr DM (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann Bot (Lond) 90: 631-636.
78. Pressman E, Shaked R, Shen S, Altahan L, Firon N (2012) Variations in carbohydrate content and sucrose-metabolizing enzymes in tomato (Solanum lycopersicum L.) stamen parts during pollen maturation. Am J Plant Sci 3: 252-260.
79. Proels RK, Gonzalez MC, Roitsch T (2006) Gibberellin-dependent induction of tomato extracellular invertase Lin7 is required for pollen development. Funct Plant Biol 33: 547-554.
80. Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3: 942-955.
81. Ruberti C, Brandizzi F (2014) Conserved and plant-unique strategies for overcoming endoplasmic reticulum stress. Front Plant Sci 5: 69
82. Saini HS, Sedgley M, Aspinall D (1984) Developmental anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Aust J Plant Physiol 11: 243-253.
83. Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, Miyazawa Y, Takahashi H, Watanabe M, Higashitani A (2010) Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci USA 107: 8569-8574.
84. Sato S, Kamiyama M, Iwata T, Makita N, Furukawa H, Ikeda H (2006) Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann Bot (Lond) 97: 731-738.
85. Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819: 104-119.
86. Schoper JB, Lambert RJ, Vasilas BL, Westgate ME (1987) Plant factors controlling seed set in maize : the influence of silk, pollen, and ear-leaf water status and tassel heat treatment at pollination. Plant Physiol 83: 121-125.
87. Selinski J, Scheibe R (2014) Pollen tube growth: where does the energy come from? Plant Signal Behav 9: e977200
88. Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28: 269-277.
89. Sharma KD, Nayyar H (2016) Regulatory networks in pollen development under cold stress. Front Plant Sci 7: 402
90. Sheoran IS, Sproule KA, Olson DJH, Ross ARS, Sawhney VK (2006) Proteome profile and functional classification of proteins in Arabidopsis thaliana (Landsberg erecta) mature pollen. Sex Plant Reprod 19: 185-196.
91. Singh A, Grover A (2008) Genetic engineering for heat tolerance in plants. Physiol Mol Biol Plants 14: 155-166.
92. Srivastava R, Deng Y, Shah S, Rao AG, Howell SH (2013) BINDING PROTEIN is a master regulator of the endoplasmic reticulum stress sensor/transducer bZIP28 in Arabidopsis. Plant Cell 25: 1416-1429.
93. Suzuki K, Takeda H, Tsukaguchi T, Egawa Y (2001) Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress. Sex Plant Reprod 13: 293-299.
94. Tang RS, Zheng JC, Jin ZQ, Zhang D, Huang H, Chen LG (2008) Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA, GAs and ABA in rice (Oryza sativa L.). Plant Growth Regul 54: 37-43.
95. Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT, Rato C, Poulsen LR, McDowell S, Miller G, Mittler R, Harper JF (2013) A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 161: 1010-1020.
96. Vierling E (1991) The roles of heat-shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579-620.
97. Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stressinduced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61: 733-746.
98. Wang L, Ruan YL (2016) Critical roles of vacuolar invertase in floral organ development and male and female fertilities are revealed through characterization of GhVIN1-RNAi cotton plants. Plant Physiol 171: 405-423
99. Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26: 2007-2023.
100. Yi J, Moon S, Lee YS, Zhu L, Liang W, Zhang D, Jung KH, An G (2016) Defective Tapetum Cell Death 1 (DTC1) regulates ROS levels by binding to metallothionein during tapetum degeneration. Plant Physiol 170: 1611-1623.
101. Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, et al (2009) RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol 150: 1204-1218.
102. Zhang X, Li J, Liu A, Zou J, Zhou X, Xiang J, Rerksiri W, Peng Y, Xiong X, Chen X (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS One 7: e49652
103. Zhang XW, Xiong HR, Liu AL, Zhou XY, Peng Y, Li ZX, Luo GY, Tian XR, Chen XB (2014) Microarray data uncover the genome-wide gene expression patterns in response to heat stress in rice post-meiosis panicle. J Plant Biol 57: 327-336.