Temperature stress and plant sexual reproduction: Uncovering the weakest links

Journal of Experimental Botany

Volumn 61, Issue 7, 2010, Pages 1959-1968

  Zinn, Kelly E ^a   Tunc Ozdemir, Meral ^a   Harper, Jeffrey F ^a  

^a UNIVERSITY OF NEVADA   (United States)

Author keywords

Cold stress; Fertilization; Gene expression; Heat stress; Plant reproduction; Pollen; Pollen tropism; Seed set

Indexed keywords

BIOLOGICAL MODEL; FERTILIZATION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POLLEN; REVIEW; TEMPERATURE;

FERTILIZATION; GENE EXPRESSION PROFILING; MODELS, BIOLOGICAL; POLLEN; STRESS, PHYSIOLOGICAL; TEMPERATURE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAGNOLIOPHYTA;

EID: 77951870928     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq053     Document Type: Review

References (88)

1. Allen DJ, Ort DR. 2001. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science 6, 36-42.
2. 2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. Physiologia Plantarum 112, 505-512.
3. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399.
4. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. 2006. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. Plos Genetics 2, 980-989.
5. Baniwal SK, Bharti K, Chan KY, et al. 2004. Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences 29, 471-487.
6. Barnabás B, Jager K, Feher A. 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell and Environment 31, 11-38.
7. Battisti DS, Naylor RL. 2009. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240-244.
8. Blum A, Sinmena B, Mayer J, Golan G, Shpiler L. 1994. Stem reserve mobilization supports wheat-grain filling under heat-stress. Australian Journal of Plant Physiology 21, 771-781.
9. Borg M, Brownfield L, Twell D. 2009. Male gametophyte development: a molecular perspective. Journal of Experimental Botany 60, 1465-1478.
10. Busch W, Wunderlich M, Schoffl F. 2005. Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. The Plant Journal 41, 1-14.
11. Charles WB, Harris RE. 1972. Tomato fruit-set at high and low-temperatures. Canadian Journal of Plant Science 52, 497-506.
12. Chinnusamy V, Zhu J, Zhu JK. 2007. Cold stress regulation of gene expression in plants. Trends in Plant Science 12, 444-451.
13. Craufurd PQ, Wheeler TR. 2009. Climate change and the flowering time of annual crops. Journal of Experimental Botany 60, 2529-2539.
14. Croser JS, Clarke HJ, Siddique KHM, Khan TN. 2003. Low-temperature stress: implications for chickpea (Cicer arietinum L.) improvement. Critical Reviews in Plant Sciences 22, 185-219.
15. Dong YS, Zhao LM, Liu B, Wang ZW, Jin ZQ, Sun H. 2004. The genetic diversity of cultivated soybean grown in China. Theoretical and Applied Genetics 108, 931-936.
16. 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 Physiology 94, 665-670.
17. Fischer G, Shah M, Tubiello FN, van Velhuizen H. 2005. Socio-economic and climate change impacts on agriculture: an integrated assessment, 1990-2080. Philosophical Transactions of the Royal Society B-Biological Sciences 360, 2067-2083.
18. Fowler S, Thomashow MF. 2002. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. The Plant Cell 14, 1675-1690.
19. 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. Journal of Experimental Botany 60, 3891-3908.
20. Funatsuki H, Ohnishi S. 2009. Recent advances in physiological and genetic studies on chilling tolerance in soybean. Jarq-Japan Agricultural Research Quarterly 43, 95-101.
21. Gounaris K, Brain ARR, Quinn PJ, Williams WP. 1984. Structural reorganization of chloroplast thylakoid membranes in response to heat-stress. Biochimica et Biophysica Acta 766, 198-208.
22. Grobei MA, Qeli E, Brunner E, Rehrauer H, Zhang R, Roschitzki B, Basler K, Ahrens CH, Grossniklaus U. 2009. Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function. Genome Research 19, 1786-1800.
23. Hayase H, Satake T, Nishiyama I, Ito N. 1969. Male sterility caused by cooling treatment at the meiotic stage in rice plants. II. The most sensitive stage to cooling and the fertilising ability of pistils. Proceedings of the Crop Science Society of Japan 38, 706-711.
24. Hedhly A, Hormaza JI, Herrero M. 2005. The effect of temperature on pollen germination, pollen tube growth, and stigmatic receptivity in peach. Plant Biology 7, 476-483.
25. Hedhly A, Hormaza JI, Herrero M. 2008. Global warming and plant sexual reproduction. Trends in Plant Science 14, 30-36.
26. Herrero M. 2003. Male and female synchrony and the regulation of mating in flowering plants. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 358, 1019-1024.
27. Herrero M, Arbeloa A. 1989. Influence of the pistil on pollen-tube kinetics in peach (Prunus persica). American Journal of Botany 76, 1441-1447.
28. Herrero MP, Johnson RR. 1980. High-temperature stress and pollen viability of maize. Crop Science 20, 796-800.
29. Honys D, Twell D. 2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biology 5, R85.
30. Hopf N, Plesofskyvig N, Brambl R. 1992. The heat-shock response of pollen and other tissues of maize. Plant Molecular Biology 19, 623-630.
31. Howarth CJ. 2005. Genetic improvements of tolerance to high temperature. In: Ashraf M, Harris PJC, eds. Abiotic stresses: plant resistance through breeding and molecular approaches. New York: Haworth Press Inc., 277-300.
32. Iba K. 2002. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annual Review of Plant Biology 53, 225-245.
33. 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.). Journal of Experimental Botany 61, 143-156.
34. Jain M, Prasad PVV, Boote KJ, Hartwell AL, 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.
35. Jakobsen HB, Martens H. 1994. Influence of temperature and aging of ovules and pollen on reproductive success in Trifolium repens L. Annals of Botany 74, 493-501.
36. Kakani VG, Prasad PVV, Craufurd PQ, Wheeler TR. 2002. Response of in vitro pollen germination and pollen tube growth of groundnut (Arachis hypogaea L.) genotypes to temperature. Plant, Cell and Environment 25, 1651-1661.
37. Kakani VG, Reddy KR, Koti S, Wallace TP, Prasad PVV, Reddy VR, Zhao D. 2005. Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Annals of Botany 96, 59-67.
38. Kim SJ, Lee SC, Hong SK, An K, An G, Kim SR. 2009. Ectopic expression of a cold-responsive OsAsr1 cDNA gives enhanced cold tolerance in transgenic rice plants. Molecules and Cells 27, 449-458.
39. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD. 2007. Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310-316.
40. Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF. 2002. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130, 2129-2141.
41. Larkindale J, Vierling E. 2008. Core genome responses involved in acclimation to high temperature. Plant Physiology 146, 748-761.
42. Law RD, Crafts-Brandner SJ. 1999. Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173-181.
43. Lee BH, Henderson DA, Zhu JK. 2005. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. The Plant Cell 17, 3155-3175.
44. Lee JY, Lee DH. 2003. Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiology 132, 517-529.
45. Lin ZF, Zhong SL, Grierson D. 2009. Recent advances in ethylene research. Journal of Experimental Botany 60, 3311-3336.
46. Lord EM. 2003. Adhesion and guidance in compatible pollination. Journal of Experimental Botany 54, 47-54.
47. Ma SY, Wu WH. 2007. AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Molecular Biology 65, 511-518.
48. Malhó R, Liu Q, Monteiro D, Rato C, Camacho L, Dinis A. 2006. Signalling pathways in pollen germination and tube growth. Protoplasma 228, 21-30.
49. Matsui T, Omasa K. 2002. Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Annals of Botany 89, 683-687.
50. Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15-19.
51. Morrison MJ, Stewart DW. 2002. Heat stress during flowering in summer Brassica. Crop Science 42, 797-803.
52. Myers C, Romanowsky SM, Barron YD, Garg S, Azuse CL, Curran A, Davis RM, Hatton J, Harmon AC, Harper JF. 2009. Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. The Plant Journal 59, 528-539.
53. Oliver SN, Dennis ES, Dolferus R. 2007. ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant and Cell Physiology 48, 1319-1330.
54. Oliver SN, Van Dongen JT, Alfred SC, et al. 2005. Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant, Cell and Environment 28, 1534-1551.
55. Park SY, Fung P, Nishimura N, et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071.
56. Peet MM, Sato S, Gardner RG. 1998. Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant, Cell and Environment 21, 225-231.
57. Pina C, Pinto F, Feijo JA, Becker JD. 2005. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiology 138, 744-756.
58. Prasad PVV, Craufurd PQ, Summerfield RJ. 1999. Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress. Annals of Botany 84, 381-386.
59. Putterill J, Laurie R, Macknight R. 2004. It's time to flower: the genetic control of flowering time. Bioessays 26, 363-373.
60. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R. 2009. Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genetics 5, e1000621.
61. Rosenzweig CA, Iglesias XB, Yang PR, Epstein E, Chivian E. 2001. Climate change and extreme weather events. Implications for food production, plant diseases and pest. Global Change and Human Health 2, 90-104.
62. Saini HS, Sedgley M, Aspinall D. 1983. Effect of heat-stress during floral development on pollen-tube growth and ovary anatomy in wheat (Triticum aestivum L.). Australian Journal of Plant Physiology 10, 137-144.
63. Saini HS, Sedgley M, Aspinall D. 1984. Developmental anatomy in wheat of male-sterility induced by heat-stress, water deficit or abscisic-acid. Australian Journal of Plant Physiology 11, 243-253.
64. Sakata T, Takahashi H, Nishiyama I, Higashitani A. 2000. Effects of high temperature on the development of pollen mother cells and microspores in barley Hordeum vulgare L. Journal of Plant Research 113, 395-402.
65. Salem MA, Kakani VG, Koti S, Reddy KR. 2007. Pollen-based screening of soybean genotypes for high temperatures. Crop Science 47, 219-231.
66. Sataka T, Hayase H. 1970. Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimation of pollen developmental stage and the most sensitive stage to coolness. Proceedings of the Crop Science Society of Japan 39, 468-473.
67. Sato S, Peet MM, Thomas JF. 2002. Determining critical pre-and post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures. Journal of Experimental Botany 53, 1187-1195.
68. Singh SK, Kakani VG, Brand D, Baldwin B, Reddy KR. 2008. Assessment of cold and heat tolerance of winter-grown canola (Brassica napus L.) cultivars by pollen-based parameters. Journal of Agronomy and Crop Science 194, 225-236.
69. Smith SD, Nowak RS. 1990. Ecophysiology of plants in the intermountain lowlands. In: Osmond CB, Pitelka LF, Hidy GM, eds. Plant biology of the basin and range. New York: Springer-Verlag, 179-241.
70. Snedden WA, Fromm H. 2001. Calmodulin as a versatile calcium signal transducer in plants. New Phytologist 151, 35-66.
71. Snider JL, Oosterhuis DM, Skulman BW, Kawakami EM. 2009. Heat stress-induced limitations to reproductive success in Gossypium hirsutum. Physiologia Plantarum 137, 125-138.
72. Solomon S, Qin D, Manning M, Marquis M, Averyt K, Tignor MMB, Miller HL, Cheng Z. 2007. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. New York: Cambridge University Press.
73. Srinivasan A, Saxena NP, Johansen C. 1999. Cold tolerance during early reproductive growth of chickpea (Cicer arietinum L.): genetic variation in gamete development and function. Field Crops Research 60, 209-222.
74. Strasser BJ. 1997. Donor side capacity of Photosystem II probed by chlorophyll a fluorescence transients. Photosynthesis Research 52, 147-155.
75. Suzuki N, Mittler R. 2006. Reactive oxygen species and temperature stresses: a delicate balance between signalling and destruction. Physiologia Plantarum 126, 45-51.
76. Takeoka Y, Hiroi K, Kitano H, Wada T. 1991. Pistil hyperplasia in rice spikelets as affected by heat-stress. Sexual Plant Reproduction 4, 39-43.
77. Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H. 2010. Cold stress effects on reproductive development in grain crops: an overview. Environmental and Experimental Botany 67, 429-443.
78. Thomashow MF. 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571-599.
79. Tonsor SJ, Scott C, Boumaza I, Liss TR, Brodsky JL, Vierling E. 2008. Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Molecular Ecology 17, 1614-1626.
80. Wahid A, Gelani S, Ashraf M, Foolad MR. 2007. Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199-223.
81. Wang WX, Vinocur B, Altman A. 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1-14.
82. Wang WX, Vinocur B, Shoseyov O, Altman A. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9, 244-252.
83. Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH. 2008. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiology 148, 1201-1211.
84. Whittle CA, Otto SP, Johnston MO, Krochko JE. 2009. Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany-Botanique 87, 650-657.
85. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781-803.
86. Yang CY, Chen YC, Jauh GY, Wang CS. 2005. A lily ASR protein involves abscisic acid signalling and confers drought and salt resistance in Arabidopsis. Plant Physiology 139, 836-846.
87. Young LW, Wilen RW, Bonham-Smith PC. 2004. High temperature stress of Brassica napus during flowering reduces micro-and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany 55, 485-495.
88. Zhu SY, Yu XC, Wang XJ, et al. 2007. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. The Plant Cell 19, 3019-3036.