Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance

Frontiers in Plant Science

Volumn 4, Issue AUG, 2013, Pages

  Bokszczanin, Kamila L ^a   Fragkostefanakis, Sotirios ^b  

^a GENXPRO GMBH   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Epigenetic; Heat stress; Metabolomic; Pollen; Proteomic; Thermotolerance; Transcriptomic

Indexed keywords

EID: 84900505705     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00315     Document Type: Review

References (269)

1. Aarts, M. G. M., Hodge, R., Kalan-tidis, K., Florack, D., Wilson, Z. A., Mulligan, B. J., et al. (1997). The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J. 12, 615-623. doi: 10.1046/j.1365-313X.1997.d01-8.x
2. Abiko, M., Akibayashi, K., Sakata, T., Kimura, M., Kihara, M., Itoh, K., et al. (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. doi: 10.1007/s00497-005-0004-2
3. Achkor, H., Diaz, M., Fernandez, M. R., Biosca, J. A., Pares, X., and Martinez, M. C. (2003). Enhanced formaldehyde detoxification by over-expression of glutathione-dependent formaldehyde dehydrogenase from Arabidopsis. Plant Physiol. 132, 2248-2255. doi: 10.1104/pp.103.022277
4. Ahmed, F. E., Hall, A. E., and Dema-son, D. A. (1992). Heat injury during floral development in Cow-pea (Vigna-Unguiculata, Fabaceae). Am. J. Bot. 79, 784-791. doi: 10.2307/2444945
5. Ahuja, I., De Vos, R. C., Bones, A. M., and Hall, R. D. (2010). Plant molecular stress responses face climate change. Trends Plant Sci. 15, 664-674. doi: 10.1016/j.tplants.2010.08.002
6. Allakhverdiev, S. I., Los, D. A., Mohanty, P., Nishiyama, Y., and Murata, N. (2007). Glycinebetaine alleviates the inhibitory repair of photosystem II effect of moderate heat stress on the during photoinhibition. Biochim. Biophys. Acta 1767, 1363-1371. doi: 10.1016/j.bbabio.2007.10.005
7. Allwood, J., and Goodacre, R. (2010). An Introduction to liquid chromatography-mass spectrom-etry instrumentation applied in plant metabolomic analyses. Phytochem. Anal. 21, 33-47. doi: 10.1002/pca. 1187
8. Aloni, B., Peet, M., Pharr, M., and Karni, L. (2001). 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. 112, 505-512. doi: 10.1034/j.1399-3054.2001.1120407.x
9. Angers, B., Castonguay, E., and Mas-sicotte, R. (2010). Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol. Ecol. 19, 1283-1295. doi: 10.1111/j.1365-294X.2010.04580.x
10. Annan, R. S., Kresbach, G. M., Giese, R. W., and Vouros, P. (1989). Trace detection of modified DNA bases via moving-belt liquid chromatography-mass spec-trometry using electrophoric derivatization and negative chemical ionization. J. Chromatogr. 465, 285-296. doi: 10.1016/S0021-9673(01) 92666-4
11. Arumuganathan, K., Martin, G. B., Telenius, H., Tanksley, S. D., and Earle, E. D. (1994). Chromosome 2-specific DNA clones from flow-sorted chromosomes of tomato. Mol. Gen. Genet. 242, 551-558. doi: 10.1007/BF00285278
12. Atkinson, B. G., Raizada, M., Bouchard, R. A., Frappier, J. R. H., and Walden, D. B. (1993). The independent stage-specific expression of the 18-Kda heat-shock protein genes during microsporogenesis in Zea-Mays L. Dev. Genet. 14, 15-26. doi: 10.1002/dvg.1020140104
13. Baniwal, S. K., Chan, K. Y., Scharf, K. D., and Nover, L. (2007). Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282, 3605-3613. doi: 10.1074/jbc.M609545200
14. Barnabás, B., Jager, K., and Feher, A. (2008). The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 31, 11-38. doi: 10.1111/j.1365-3040.2007.01727.x
15. Becker, J. D., Boavida, L. C., Carneiro, J., Haury, M., and Feijo, J. A. (2003). Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen tran-scriptome. Plant Physiol. 133, 713-725. doi: 10.1104/pp.103.028241
16. Bhadula, S. K., Elthon, T. E., Habben, J. E., Helentjaris, T. G., Jiao, S. P., and Ristic, Z. (2001). Heat-stress induced synthesis of chloroplast protein synthesis elongation factor (EF-Tu) in a heat-tolerant maize line. Planta 212, 359-366. doi: 10.1007/ s004250000416
17. Bita, C. E., Zenoni, S., Vriezen, W. H., Mariani, C., Pezzotti, M., and Gerats, T. (2011). Temperature stress differentially modulates transcription in meiotic anthers of heat-tolerant and heat-sensitive tomato plants. BMC Genomics 12:384. doi: 10.1186/1471-2164-12-384
18. Boston, R. S., Viitanen, P. V., and Vierling, E. (1996). Molecular chap-erones and protein folding in plants. Plant Mol. Biol. 32, 191-222. doi: 10.1007/BF00039383
19. Bouchard, R. A. (1990). Characterization of expressed meiotic prophase repeat transcript clones of lilium -meiosis-specific expression, relat-edness, and affinities to small heat-shock protein genes. Genome 33, 68-79. doi: 10.1139/g90-012
20. Bouché, N., and Fromm, H. (2004). GABA in plants: just a metabolite? Trends Plant Sci. 9, 110-115. doi: 10.1016/j.tplants.2004.01.006
21. Brown, J. A., Li, D., Alic, M., and Gold, M. H. (1993). Heat-shock induction of manganese peroxidase gene-transcription in phaneroch-aete-chrysosporium. Appl. Environ. Microbiol. 59, 4295-4299.
22. Bukau, B., Weissman, J., and Horwich, A. (2006). Molecular chaperones and protein quality control. Cell 125, 443-451. doi: 10.1016/j.cell.2006.04.014
23. Busch, W., Wunderlich, M., and Schoffl, F. (2005). Identification of novel heat shock factor-dependent genes and biochemical pathways in Ara- bidopsis thaliana. Plant J. 41, 1-14. doi: 10.1111/j.1365-313X.2004.02272.x
24. Calarco, J. P., Borges, F., Donoghue, M. T. A., Van Ex, F., Jullien, P. E., Lopes, T., et al. (2012). Reprogramming of DNA methy-lation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194-205. doi: 10.1016/j.cell.2012. 09.001
25. Cartagena, J. A., Matsunaga, S., Seki, M., Kurihara, D., Yokoyama, M., Shinozaki, K., et al. (2008). The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev. Biol. 315, 355-368. doi: 10.1016/j.ydbio.2007.12.016
26. Chakraborty, U., and Tongden, C. (2005). Evaluation of heat acclimation and salicylic acid treatments as potent inducers of thermotolerance in Cicer arietinum L. Curr. Sci. 89, 384-389.
27. Chalker-Scott, L. (2002). Do antho-cyanins function as osmoregulators in leaf tissues? Adv. Bot. Res. 37, 103-127. doi: 10.1016/S0065-2296(02)37046-0
28. Charng, Y. Y., Liu, H. C., Liu, N. Y., Chi, W. T., Wang, C. N., Chang, S. H., et al. (2007). A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Ara-bidopsis. Plant Physiol. 143, 251-262. doi: 10.1104/pp.106.091322
29. Chaturvedi, P., Ischebeck, T., Egelhofer, V., Lichtscheidl, I., and 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. doi: 10.1021/pr400197p [Epub ahead of print].
30. Che, P., Bussell, J. D., Zhou, W. X., Estavillo, G. M., Pogson, B. J., and Smith, S. M. (2010). Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Ara-bidopsis. Sci. Signal. 3, ra69. doi: 10.1126/scisignal.2001140
31. Cheikh, N., and Jones, R. N. (1994). Disruption of maize kernel growth and development by heat stress. Plant Physiol. 106, 45-51. doi: 10.1104/pp.106.1.45
32. Chen, J. P., Burke, J. J., Velten, J., and Xin, Z. U. (2006). FtsH11 protease plays a critical role in Arabidopsis thermo-tolerance. Plant J. 48, 73-84. doi: 10.1111/j.1365-313X.2006.02855.x
33. Chen, Y. C., and McCormick, S. (1996). Sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development 122, 3243-3253.
34. Chiusano, M. L., D'Agostino, N., Traini, A., Licciardello, C., Raimondo, E., Aversano, M., et al. (2008). ISOL@: an Italian SOLAnaceae genomics resource. BMC Bioinformatics 9, S7. doi: 10.1186/1471-2105-9-S2-S7
35. Cho, E. K., and Choi, Y. J. (2009). A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol. Lett. 31, 597-606. doi: 10.1007/s10529-008-9880-5
36. Chu, T. M., Aspinall, D., and Paleg, L. G. (1974). Stress metabolism. VI. Temperature stress and the accumulation of proline in barley and radish. Aust. J. Plant Physiol. 1, 87-97. doi: 10.1071/PP9740087
37. Clapier, C. R., and Cairns, B. R. (2009). The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304. doi: 10.1146/annurev. biochem.77.062706.153223
38. Clément, C., Chavant, L., Burrus, M., and Audran, J. C. (1994). Anther starch variations in Lilium during pollen development. Sex. Plant Reprod. 7, 347-356. doi: 10.1007/ BF00230513
39. Coberly, L. C., and Rausher, M. D. (2003). Analysis of a chalcone synthase mutant in Ipomoea pur-purea reveals a novel function for flavonoids: amelioration of heat stress. Mol. Ecol. 12, 1113-1124. doi: 10.1046/j.1365-294X.2003.01786.x
40. Conde, A., Chaves, M. M., and Geros, H. (2011). Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 52, 1583-1602. doi: 10.1093/pcp/pcr107
41. Craufurd, P. Q., and Peacock, J. M. (1993). Effect of heat and drought stress on Sorghum (Sorghum-Bicolor). 2. Grain-yield. Exp. Agric. 29, 77-86. doi: 10.1017/ S0014479700020421
42. Craufurd, P. Q., and Wheeler, T. R. (2009). Climate change and the flowering time of annual crops. J. Exp. Bot. 60, 2529-2539. doi: 10.1093/jxb/erp196
43. Cukkemane, A., Seifert, R., and Kaupp, U. B. (2011). Cooperative and uncooperative cyclic-nucleotide-gated ion channels. Trends Biochem. Sci. 36, 55-64. doi: 10.1016/j.tibs.2010. 07.004
44. Cvikrová, M., Gemperlova, L., Dobra, J., Martincova, O., Prasil, I. T., Gubis, J., et al. (2012). Effect of heat stress on polyannine metabolism in proline-over-producing tobacco plants. Plant Sci. 182, 49-58. doi: 10.1016/j.plantsci.2011.01.016
45. Dai, S., Li, L., Chen, T., Chong, K., Xue, Y., and Wang, T. (2006). Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6, 2504-2529. doi: 10.1002/pmic.2004 01351
46. Dai, S. J., and Chen, S. X. (2012). Single-cell-type Proteomics: toward a holistic understanding of plant function. Mol. Cell. Proteomics 11, 1622-1630. doi: 10.1074/mcp.R112.021550
47. Dai, S. J., Chen, T. T., Chong, K., Xue, Y. B., Liu, S. Q., and Wang, T. (2007). Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol. Cell. Proteomics 6, 207-230. doi: 10.1074/mcp.M600146-MCP200
48. Dang, F. F., Wang, Y. N., Yu, L., Eulgem, T., Lai, Y., Liu, Z. Q., et al. (2013). CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ. 36, 757-774. doi: 10.1111/pce.12011
49. Datta, R., Chamusco, K. C., and Chourey, P. S. (2002). Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol. 130, 1645-1656. doi: 10.1104/pp.006908
50. de Koning, B., Blombach, F., Wu, H., Brouns, S. J. J., and Van Der Oost, J. (2009). Role of multiprotein bridging factor 1 in archaea: bridging the domains? Biochem. Soc. Trans. 37, 52-57. doi: 10.1042/BST0370052
51. Deng, Y., Humbert, S., Liu, J. X., Srivas-tava, R., Rothstein, S. J., and How-ell, S. H. (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. U.S.A. 108, 7247-7252. doi: 10.1073/pnas.1102117108
52. Deng, Y., Srivastava, R., and How-ell, S. H. (2013). Endoplasmic retic-ulum (ER) stress response and its physiological roles in plants. Int. J. Mol. Sci. 14, 8188-8212. doi: 10.3390/ijms14048188
53. Derksen, J., Van Wezel, R., Knuiman, B., Ylstra, B., and Van Tunen, A. J. (1999). Pollen tubes of flavonol-deficient Petunia show striking alterations in wall structure leading to tube disruption. Planta 207, 575-581. doi: 10.1007/s004250050520
54. de Ronde, J. A., Cress, W. A., Kruger, G. H. J., Strasser, R. J., and Van Staden, J. (2004). Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J. Plant Physiol. 161, 1211-1224. doi: 10.1016/j.jplph.2004.01.014
55. de Ronde, J. A., Spreeth, M. H., and Cress, W. A. (2000). Effect of antisense L-Delta(1)-pyrroline-5-carboxylate reductase transgenic soybean plants subjected to osmotic and drought stress. Plant Growth Regul. 32, 13-26. doi: 10.1023/A: 1006338911617
56. Diamant, S., Eliahu, N., Rosenthal, D., and Goloubinoff, P. (2001). Chemical chaperones regulate molecular chap-erones in vitro and in cells under combined salt and heat stresses. J. Biol. Chem. 276, 39586-39591. doi: 10.1074/jbc.M103081200
57. Erickson, A. N., and Markhart, A. H. (2002). Flower developmental stage and organ sensitivity of bell pepper (Capsicum annuum L.) to elevated temperature. Plant Cell Environ. 25, 123-130. doi: 10.1046/j.0016-8025.2001.00807.x
58. Erkina, T. Y., Tschetter, P. A., and Erkine, A. M. (2008). Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes. Mol. Cell. Biol. 28, 1207-1217. doi: 10.1128/MCB.01069-07
59. Erkina, T. Y., Zou, Y., Freeling, S., Vorobyev, V. I., and Erkine, A. M. (2010). Functional interplay between chromatin remodeling complexes RSC, SWI/SNF and ISWI in regulation of yeast heat shock genes. Nucleic Acids Res. 38, 1441-1449. doi: 10.1093/nar/gkp1130
60. Fahlgren, N., Sullivan, C. M., Kasschau, K. D., Chapman, E. J., Cumbie, J. S., Montgomery, T. A., et al. (2009). Computational and analytical frame-workforsmallRNA profiling by high-throughput sequencing. RNA 15, 992-1002. doi: 10.1261/rna.1473809
61. Feechan, A., Kwon, E., Yun, B. W., Wang, Y., Pallas, J. A., and Loake, G. J. (2005). A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. U.S.A. 102, 8054-8059. doi: 10.1073/pnas.0501456102
62. Ferreira, S., Hjerno, K., Larsen, M., Wingsle, G., Larsen, P., Fey, S., et al. (2006). Proteome profiling of Populus euphratica Oliv. Upon heat stress. Ann. Bot. 98, 361-377. doi: 10.1093/aob/mcl106
63. Finka, A., Mattoo, R. U., and Goloubinoff, P. (2011). Meta-analysis of heat- and chemically upregu-lated chaperone genes in plant and human cells. Cell Stress Chaperones 16, 15-31. doi: 10.1007/s12192-010-0216-8
64. Firon, N., Pressman, E., Meir, S., Khoury, R., and Altahan L. (2012). Ethylene is involved in maintaining tomato (Solatium lycopersicum) pollen quality under heat-stress conditions. AoB Plants doi: 10.1093/aob-pla/pls024
65. Firon, N., Shaked, R., Peet, M. M., Pharr, D. M., Zamski, E., Rosen-feld, K., et al. (2006). Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sei Hortic. 109, 212-217. doi: 10.1016/j.scienta.2006.03.007
66. /-deoxycytidine in genomic DNA: application to plant, animal and human cancer tissues. Electrophoresis 23, 1677-1681. doi: 10.1002/1522-2683(200206)23:11<1677::AID-ELPS1677>3.0.CO;2-Z
67. Frank, G., Pressman, E., Ophir, R., Althan, L., Shaked, R., Freedman, M., et al. (2009). Transcriptional profiling of maturing tomato (Solatium lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. Exp. Bot 60, 3891-3908. doi: 10.1093/jxb/erp234
68. Frommer, M., Mcdonald, L. E., Millar, D. S., Collis, C. M., Watt, F., Grigg, G. W.,et al. (1992). A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sei U.S.A. 89, 1827-1831. doi: 10.1073/pnas.89.5.1827
69. Fu, J. M., Momcilovic, I., Clemente, T. E., Nersesian, N., Trick, H. N., and Ristic, Z. (2008). Het-erologous expression of a plastid EF-Tu reduces protein thermal aggregation and enhances CO(2) fixation in wheat (Triticum aestivum) following heat stress. Plant Mol. Biol. 68, 277-288. doi: 10.1007/s11103-008-9369-6
70. Gao, H. B., Brandizzi, F., Ben-ning, C., and Larkin, R. M. (2008). A membrane-tethered transcription factor defines a branch of the heat stress response in Ara-bidopsis thaliana. Proc. Natl. Acad. Sei U.S.A. 105, 16398-16403. doi: 10.1073/pnas.0808463105
71. Georgieva, K., Tsonev, T., Velikova, V., and Yordanov, I. (2000). Photo-synthetic activity during high temperature treatment of pea plants. Plant Physiol. 157, 169-176. doi: 10.1016/S0176-1617(00)80187-X
72. German, M. A., Pillay, M., Jeong, D. H., Hetawal, A., Luo, S., Janardhanan, P., et al. (2008). Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26, 941-946. doi: 10.1038/nbt1417
73. Ginzberg, I., Barel, G., Ophir, R., Tzin, E., Tanami, Z., Muddarangappa, T., et al. (2009). Transcriptomic profiling of heat-stress response in potato periderm. J. Exp. Bot. 60, 4411-4421. doi: 10.1093/jxb/erp281
74. Giorno, F., Wolters-Arts, M., Grillo, S., Scharf, K. D., Vriezen, W. H., and 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. doi: 10.1093/jxb/ erp316
75. Gonzalez-Perez, S., Gutierrez, J., GarciaGarcia, F., Osuna, D., Dopazo, J., Lorenzo, O., et al. (2011). Early tran-scriptional defense responses in Ara-bidopsis cell suspension culture under high-light conditions. Plant Physiol. 156, 1439-1456. doi: 10.1104/pp. 111.177766
76. Grobei, M. A., Qeli, E., Brunner, E., Rehrauer, H., Zhang, R. X., Ros-chitzki, B., et al. (2009). Deterministic protein inference for shotgun pro-teomics data provides new insights into Arabidopsis pollen development and function. Genome Res. 19, 1786-1800. doi: 10.1101/gr.089060.108
77. Grover, A., Mittal D., Negi, M., and Lavania, D. (2013). Generating high temperature tolerant trans-genic plants: achievements and challenges. Plant Sci. 205-206, 38-47. doi: 10.1016/j.plantsci.2013.01.005
78. Hahn, A., Bublak, D., Schleiff, E., and Scharf, K. D. (2011). Crosstalk between Hsp90 and Hsp70 chaper-ones and heat stress transcription factors in tomato. Plant Cell 23, 741-755. doi: 10.1105/tpc.110.076018
79. Halket, J. M., Waterman, D., Przy-borowska, A. M., Patel, R. K. P., Fraser, P. D., and Bramley, P. M. (2005). Chemical derivatization and mass spectral libraries in metabolic profiling by GC/MS and LC/MS/MS. J. Exp. Bot. 56, 219-243. doi: 10.1093/ jxb/eri069
80. Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141, 312-322. doi: 10.1104/pp.106.077073
81. Hare, P. D., Cress, W. A., and Van Staden, J. (1998). Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21, 535-553. doi: 10.1046/j.1365-3040.1998.00309.x
82. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011). Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332. doi: 10.1038/nature10317
83. Hartl, F. U., and Hayer-Hartl, M. (2009). Converging concepts of protein folding in vitro and in vivo. Nat. Struct Mol Biol. 16, 574-581. doi: 10.1038/nsmb.1591
84. Hatfield, J. L., Boote, K. J., Kimball, B. A., Ziska, L. H., Izaurralde, R. C, Ort, D., et al. (2011). Climate impacts on agriculture: implications for crop production. Agron. J. 103, 351-370.
85. Havaux, M. (1998). Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci. 3, 147-151. doi: 10.1016/S1360-1385(98)01200-X
86. Heckathorn, S. A., Downs, C. A., and Coleman, J. S. (1998). Nuclear-encoded chloroplast proteins accumulate in the cytosol during severe heat stress. Int. J. Plant Sci. 159, 39-45. doi: 10.1086/297519
87. Herouart, D., Vanmontagu, M., and Inze, D. (1994). Developmental and environmental-regulation of the nicotiana-plumbaginifolia cytoso-lic Cu/Zn-superoxide dismutase promoter in transgenic tobacco. Plant Physiol. 104, 873-880. doi: 10.1104/pp.104.3.873
88. Holmes-Davis, R., Tanaka, C. K., Vensel, W. H., Hurkman, W. J., and McCormick, S. (2005). Pro-teome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5, 4864-4884. doi: 10.1002/pmic.20040 2011
89. Honys, D., and Twell, D. (2003). Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132, 640-652. doi: 10.1104/pp. 103.020925
90. Honys, D., and Twell, D. (2004). Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85. doi: 10.1186/gb-2004-5-11-r85
91. Hu, M., Yao, J., and Polyak, K. (2006). Methylation-specific digital karyotyping. Nat. Protoc. 1, 1621-1636. doi: 10.1038/nprot.2006.278
92. ; untranslated region of the At-P5R gene is involved in both tran-scriptional and post-transcriptional regulation. Plant J. 26, 157-169. doi: 10.1046/j.1365-313x.2001. 01020.x
93. Huang, B. R., and Xu, C. P. (2008). Identification and characterization of proteins associated with plant tolerance to heat stress. J. Integr. Plant Biol. 50, 1230-1237. doi: 10.1111/j.1744-7909.2008.00735.x
94. Igarashi, K., Kazama, T., Motomura, K., and Toriyama, K. (2013). Whole genomic sequencing of RT98 mitochondria derived from Oryza rufi-pogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Phys-iol. 54, 237-243. doi: 10.1093/pcp/ pcs177
95. Ikeda, M., Mitsuda, N., and Ohme-Takagi, M. (2011). Arabidopsis HsfB1 and HsfB2b act as repres-sors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol. 157, 1243-1254. doi: 10.1104/pp.111.179036
96. Im, Y. J., Ji, M., Lee, A., Killens, R., Grunden, A. M., and Boss, W. F. (2009). Expression of pyrococ-cus furiosus superoxide reductase in Arabidopsis enhances heat tolerance. Plant Physiol. 151, 893-904. doi: 10.1104/pp.109.145409
97. IPCC, (2012). Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change, eds C. B. Field, V. Barros, T. F. Stocker, D. Qin, D. J. Dokken, K. L. M. D. Ebi, et al. (Cambridge: Cambridge University Press), 582p.
98. Itai, C., Ben-Zioni, A., and Ordin, L. (1973). Correlative changes in endogenous hormone levels and shoot growth induced by short heat treatments to the root. Physiol. Plant. 29, 355-360. doi: 10.1111/j.1399-3054.1973.tb04830.x
99. Iwata, Y., Fedoroff, N. V., and Koizumi, N. (2008). Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20, 3107-3121. doi: 10.1105/tpc. 108.061002
100. Jagadish, S. V. K., Cairns, J., Lafitte, R., Wheeler, T. R., Price, A. H., and Craufurd, P. Q. (2010). Genetic analysis of heat tolerance at anthesis in rice. Crop Sci. 50, 1633-1641. doi: 10.2135/cropsci2009.09.0516
101. Jäger, K., Fábián, A., and Barnabás, B. (2008). Effect of water deficit and elevated temperature on pollen development of drought sensitive and tolerant winter wheat (Triticum aestivum L.) genotypes. Acta Biol. Szegediensis 52, 67-71.
102. Jain, M., Prasad, P. V. V., Boote, K. J., Hartwell, A. L., and Chourey, P. S. (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. doi: 10.1007/s00425-007-0595-y
103. Jiang, Y. W., and Huang, B. R. (2001). Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation. Crop Sci. 41, 436-442. doi: 10.2135/cropsci2001.412436x
104. Kabe, Y., Goto, M., Shima, D., Imai, T., Wada, T., Morohashi, K., et al. (1999). The role of human MBF1 as a transcriptional coactivator. J. Biol. Chem. 274, 34196-34202. doi: 10.1074/jbc.274.48.34196
105. Kahl, G., Molina, C., Rotter, B., Jüngling, R., Frank, A., Krezdorn, N., et al. (2012). Reduced representation sequencing of plant stress transcriptomes. J. Plant Biochem. Biotechnol. 21, 119-112. doi: 10.1007/s13562-012-0129-y
106. Kaplan, F., Kopka, J., Haskell, D. W., Zhao, W., Schiller, K. C., Gatzke, N., et al. (2004). Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136, 4159-4168. doi: 10.1104/pp.104.052142
107. Kinnersley, A. M., and Turano, F. J. (2000). Gamma aminobutyric acid (GABA)and plant responsestostress. Crit. Rev. Plant Sci. 19, 479-509. doi: 10.1016/S0735-2689(01)80006-X
108. Kosová, K., Vitamvas, P., Prasil, I. T., and Renaut, J. (2011). Plant pro-teome changes under abiotic stress -contribution of proteomics studies to understanding plant stress response. J. Proteomics 74, 1301-1322. doi: 10.1016/j.jprot.2011.02.006
109. Kotak, S., Vierling, E., Baumlein, H., and Von Koskull-Doring, P. (2007). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Ara-bidopsis. Plant Cell 19, 182-195. doi: 10.1105/tpc.106.048165
110. Krasensky, J., and Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593-1608. doi: 10.1093/jxb/err460
111. Kültz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257. doi: 10.1146/annurev.physiol. 67.040403.103635
112. Kumar, S. V., and Wigge, P. A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147. doi: 10.1016/j.cell.2009.11.006
113. Kurek, I., Chang, T. K., Bertain, S. M., Madrigal, A., Liu, L., Lassner, M. W., et al. (2007). Enhanced ther-mostability of Arabidopsis rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19, 3230-3241. doi: 10.1105/tpc.107.054171
114. Kvaalen, H., and Johnsen, O. (2008). Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytol. 177, 49-59. doi: 10.1111/j.1469-8137.2007. 02222.x
115. Langridge, P., and Fleury, D. (2011). Making the most of 'omics' for crop breeding. Trends Biotechnol. 29, 33-40. doi: 10.1016/j.tibtech.2010.09.006
116. Lansac, A. R., Sullivan, C. Y., and Johnson, B. E. (1996). Accumulation of free proline in sorghum (Sorghum bicolor) pollen. Can. J. Bot. 74, 40-45. doi: 10.1139/b96-006
117. Larkindale, J., Hall, J. D., Knight, M. R., and Vierling, E. (2005). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotol-erance. Plant Physiol. 138, 882-897. doi: 10.1104/pp.105.062257
118. Larkindale, J., and Knight, M. R. (2002). Protection against heat stress-induced oxidative damage in Ara-bidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128, 682-695. doi: 10.1104/pp.010320
119. Larkindale, J., and Vierling, E. (2008). Core genome responses involved in acclimation to high temperature. Plant Physiol. 146, 748-761. doi: 10.1104/pp.107.112060
120. Lee, D. G., Ahsan, N., Lee, S. H., Kang, K. Y., Bahk, J. D., Lee, I. J., et al. (2007). A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics 7, 3369-3383. doi: 10.1002/pmic.200700266
121. Lee, U., Wie, C., Fernandez, B. O., Feelisch, M., and Vierling, E. (2008). Modulation of nitrosative stress by S-nitrosoglutathione reduc-tase is critical for thermotoler-ance and plant growth in Arabidop-sis. Plant Cell 20, 786-802. doi: 10.1105/tpc.107.052647
122. Levy, A., Rabinowitch, H. D., and Kedar, N. (1978). Morphological and physiological characters affecting flower drop and fruit set of tomatoes at high-temperatures. Euphytica 27, 211-218. doi: 10.1007/BF00039137
123. Li, C. F., Pontes, O., El-Shami, M., Henderson, I. R., Bernatavichute, Y. V., Chan, S. W., et al. (2006). An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126, 93-106. doi: 10.1016/j.cell.2006.05.032
124. Li, S., Zhou, X., Chen, L., Huang, W., and Yu, D. (2010). Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol. Cells 29, 475-483. doi: 10.1007/s10059-010-0059-2
125. Li, S. J., Fu, Q. T., Huang, W. D., and Yu, D. Q. (2009). Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep. 28, 683-693. doi: 10.1007/s00299-008-0666-y
126. Li, Z., Yue, H. Y., and Xing, D. (2012). MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Ara-bidopsis. New Phytol. 195, 85-96. doi: 10.1111/j.1469-8137.2012.04131.x
127. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A. R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396. doi: 10.1038/nprot.2006.59
128. Liu, H. C., and Charng, Y. Y. (2012). Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response. Plant Signal. Behav. 7, 547-550. doi: 10.4161/psb. 19803
129. Liu, H. C., Liao, H. T., and Charng, Y. Y. (2011). The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ. 34, 738-751. doi: 10.1111/j.1365-3040.2011.02278.x
130. Liu, H. T., Gao, F., Li, G. L., Han, J. L., Liu, D. L., Sun, D.Y., et al. (2008). The calmodulin-binding protein kinase 3 is part of heat-shock signal trans-duction in Arabidopsis thaliana. Plant J. 55, 760-773. doi: 10.1111/j.1365-313X.2008.03544.x
131. Liu, J., Sun, N., Liu, M., Liu, J., Du, B., Wang, X., et al. (2013). An autoregulatory loop controlling Ara-bidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol. 162, 512-521. doi: 10.1104/pp.112.205864
132. Liu, J. X., and Howell, S. H. (2010). bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes inArabidopsis. Plant Cell 22, 782-796. doi: 10.1105/tpc.109.072173
133. Liu, J. X., Srivastava, R., Che, P., and Howell, S. H. (2007). An endo-plasmic reticulum stress response in Arabidopsis is mediated by prote-olytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19, 4111-4119. doi: 10.1105/tpc.106. 050021
134. Liu, Q. X., Jindra, M., Ueda, H., Hiromi, Y., and Hirose, S. (2003). Drosophila MBF1 is a co-activator for Tracheae Defective and contributes to the formation of tracheal and nervous systems. Development 130, 719-728. doi: 10.1242/dev.00297
135. Liu, X., Hunag, B., and Banowetz, G. (2002). Cytokinin effects on creeping bentgrass responses to heat stress. Crop Sci. 42, 457-465. doi: 10.2135/cropsci2002.0457
136. Liu, X. Z., and Huang, B. R. (2000). Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci. 40, 503-510. doi: 10.2135/cropsci2000.402503x
137. Lobell, D.B., Schlenker, W., and CostaRoberts, J. (2011). Climate trends and global crop production since 1980. Science 333, 616-620. doi: 10.1126/science.1204531
138. Lohmann, C., Eggers-Schumacher, G., Wunderlich, M., and Schoffl, F. (2004). Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol. Genet. Genomics 271, 11-21. doi: 10.1007/s00438-003-0954-8
139. Lv, W. T., Lin, B., Zhang, M., and Hua, X. J. (2011). Proline accumulation is inhibitory to Ara-bidopsis seedlings during heat stress. Plant Physiol. 156, 1921-1933. doi: 10.1104/pp.111.175810
140. Ma, W., and Berkowitz, G. A. (2011). Ca2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytol. 190, 566-572. doi: 10.1111/j.1469-8137.2010.03577.x
141. Majoul, T., Bancel, E., Triboi, E., Ben Hamida, J., and Branlard, G. (2003). Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from total endosperm. Proteomics 3, 175-183. doi: 10.1002/pmic.200390026
142. Majoul, T., Bancel, E., Triboi, E., Ben Hamida, J., and Branlard, G. (2004). Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from non-prolamins fraction. Proteomics 4, 505-513. doi: 10.1002/pmic.200300570
143. Mallory, A. C., and Vaucheret, H. (2006). Functions of microRNAs and related small RNAs in plants. Nat. Genet. 38, S31-S36. doi: 10.1038/ng1791
144. Matsui, T., and Omasa, K. (2002). Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Ann. Bot. 89, 683-687. doi: 10.1093/aob/ mcf112
145. McNeil, S. D., Nuccio, M. L., and Hanson, A. D. (1999). Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol. 120, 945-949. doi: 10.1104/pp.120.4.945
146. Meiri, D., and Breiman, A. (2009). Ara-bidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J. 59, 387-399. doi: 10.1111/j.1365-313X.2009.03878.x
147. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev, V., et al. (2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45. doi: 10.1126/scisignal.2000448
148. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., and Mittler, R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 33, 453-467. doi: 10.1111/j.1365-3040.2009.02041.x
149. Mirouze, M., and Paszkowski, J. (2011). Epigenetic contribution to stress adaptation in plants. Curr. Opin. Plant Biol. 14, 267-274. doi: 10.1016/j.pbi.2011.03.004
150. Mishkind, M., Vermeer, J. E. M., Dar-wish, E., and Munnik, T. (2009). Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasmamembrane and nucleus. Plant J. 60, 10-21. doi: 10.1111/j.1365-313X.2009.03933.x
151. Mishra, G., Zhang, W., Deng, F., Zhao, J., and Wang, X. (2006). A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312, 264-266. doi: 10.1126/science.11 23769
152. Mishra, S. K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L., et al. (2002). In the complex family of heat stress transcription factors, HSfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555-1567. doi: 10.1101/gad.228802
153. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410. doi: 10.1016/S1360-1385(02)02312-9
154. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15-19. doi: 10.1016/j.tplants.2005. 11.002
155. Mittler, R., Finka, A., and Goloubi-noff, P. IPCC (2012). How do plants feel the heat? Trends Biochem. Sci. 37, 118-125. doi: 10.1016/ j.tibs.2011.11.007
156. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498. doi: 10.1016/j.tplants.2004.08.009
157. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., et al. (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300-309. doi: 10.1016/j.tplants.2011.03.007
158. Moco, S., Bino, R. J., De Vos, R. C. H., and Vervoort, J. (2007). Metabolomics technologies and metabolite identification. Trends Analyt. Chem. 26, 855-866. doi: 10.1016/j.trac.2007.08.003
159. Mohn, F., Weber, M., Schubeler, D., and Roloff, T. C. (2009). Methylated DNA immunoprecipita-tion (MeDIP). Methods Mol. Biol. 507, 55-64. doi: 10.1007/978-1-59745-522-0_5
160. Monton, M. R. N., and Soga, T. (2007). Metabolome analysis by capillary electrophoresis-mass spectrometry. J. Chromatogr. A 1168, 237-246. doi: 10.1016/j.chroma.2007.02.065
161. Morimoto, R. I. (1998). Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796. doi: 10.1101/gad.12.24.3788
162. Mutters, R. G., Ferreira, L. G. R., and Hall, A. E. (1989). Proline content of the anthers and pollen of heat-tolerant and heat-sensitive cowpea subjected to different temperatures. Crop Sci. 29, 1497-1500. doi: 10.2135/cropsci1989. 0011183X002900060036x
163. Nakamoto, H., and Vigh, L. (2007). The small heat shock proteins and their clients. Cell. Mol. Life Sci. 64, 294-306. doi: 10.1007/s00018-006-6321-2
164. Nakashima, K., Ito, Y., and Yamaguchi-Shinozaki, K. (2009). Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149, 88-95. doi: 10.1104/pp.108.129791
165. Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T., et al. (2004). The transcrip-tional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113-1128. doi: 10.1104/pp.103.036749
166. Neta-Sharir, I., Isaacson, T., Lurie, S., and Weiss, D. (2005). Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17, 1829-1838. doi: 10.1105/tpc.105.031914
167. Nielsen, H. B., Mundy, J., and Willenbrock, H. (2007). Functional associations by response overlap (FARO), a functional genomics approach matching gene expression phenotypes. PLoS ONE 2:e676. doi: 10.1371/journal.pone.00 00676
168. Nielsen, K., De Obaldia, A. L., and Heitman, J. (2007). Cryptococ-cus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot. Cell 6, 949-959. doi: 10.1128/EC.00097-07
169. Nishizawa, A., Yabuta, Y., and Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263. doi: 10.1104/pp.108.122465
170. Nishizawa-Yokoi, A., Yoshida, E., Yabuta, Y., and Shigeoka, S. (2009). Analysis of the regulation of target genes by an Arabidopsis heat shock transcription factor, HsfA2. Biosci. Biotechnol. Biochem. 73, 890-895. doi: 10.1271/bbb.80809
171. Noir, S., Brautigam, A., Colby, T., Schmidt, J., and Panstruga, R. (2005). A reference map of the Arabidopsis thaliana mature pollen proteome. Biochem. Biophys. Res. Commun. 337, 1257-1266. doi: 10.1016/j.bbrc.2005.09.185
172. Nover, L., Bharti, K., Doring, P., Mishra, K., Ganguli, A., and Scharf, K. D. (2001). Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6, 177-189. doi: 10.1379/1466-1268 (2001)006<0177:AATHST>2.0.CO;2
173. Ogawa, D., Yamaguchi, K., and Nishi-uchi, T. (2007). High-level overex-pression of the Arabidopsis HsfA2 gene confers not only increased the-motolerance but also salt/osmotic stress tolerance and enhanced callus growth. J. Exp. Bot. 58, 3373-3383. doi: 10.1093/jxb/erm184
174. O'Neill, L. P., and Turner, B. M. (2003). Immunoprecipitation of native chro-matin: NChIP. Methods 31, 76-82. doi: 10.1016/S1046-2023(03) 00090-2
175. Ortiz, C., and Cardemil, L. (2001). Heat-shock responses in two leguminous plants: a comparative study. J. Exp. Bot. 52, 1711-1719. doi: 10.1093/jexbot/52.361.1711
176. Peet, M. M., Sato, S., and Gardner, R. G. (1998). Comparing heat stress effects on male-fertile and malesterile tomatoes. Plant Cell Environ. 21, 225-231. doi: 10.1046/j.1365-3040.1998.00281.x
177. Perez, D. E., Hoyer, J. S., Johnson, A. I., Moody, Z. R., Lopez, J., and Kaplinsky, N. J. (2009). BOB-BER1 Is a noncanonical Arabidopsis small heat shock protein required for both evelopment and thermotoler-ance. Plant Physiol. 151, 241-252. doi: 10.1104/pp.109.142125
178. Petersen, A., Dresselhaus, T., Grobe, K., and Becker, W. M. (2006). Pro-teome analysis of maize pollen for allergy-relevant components. Proteomics 6, 6317-6325. doi: 10.1002/pmic.200600173
179. Pfender, W. F., Saha, M. C., Johnson, E. A., and Slabaugh, M. B. (2011). Mapping with RAD (restriction-site associated DNA) markers to rapidly identify QTL for stem rust resistance in Lolium perenne. Theor. Appl. Genet. 122, 1467-1480. doi: 10.1007/s00122-011-1546-3
180. Pontes, O., Li, C. F., Nunes, P. C., Haag, J., Ream, T., Vitins, A., et al. (2006). The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126, 79-92. doi: 10.1016/j.cell.2006.05.031
181. Popova, O. V., Dinh, H. Q., Aufsatz, W., and Jonak, C. (2013). The RdDM pathway is required for basal heat tolerance in Arabidopsis. Mol. Plant 6, 396-410. doi: 10.1093/mp/ sst023
182. Porch, T. G., and Jahn, M. (2001). Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris. Plant Cell Environ. 24, 723-731. doi: 10.1046/ j.1365-3040.2001.00716.x
183. Pratt, W. B., Morishima, Y., Peng, H. M., and Osawa, Y. (2010). Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp. Biol. Med. 235, 278-289. doi: 10.1258/ebm.2009.009250
184. Pressman, E., Peet, M. M., and Pharr, D. M. (2002). The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann. Bot. 90, 631-636. doi: 10.1093/aob/mcf240
185. Pressman, E., Shaked, R., and Firon N. (2007). Tomato (Lycopersicon escu-lentum) response to heat stress: focus on pollen grains. Plant Stress 1, 216-227.
186. Qin, D., Wu, H., Peng, H., Yao, Y., Ni, Z., Li, Z., et al. (2008). Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9:432. doi: 10.1186/1471-2164-9-432
187. Queitsch, C., Hong, S. W., Vierling, E., and Lindquist, S. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidop-sis. Plant Cell 12, 479-492. doi: 10.1105/tpc.12.4.479
188. Ramsahoye, B. H., Biniszkiewicz, D., Lyko, F., Clark, V., Bird, A. P., and Jaenisch, R. (2000). Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl. Acad. Sci. U.S.A. 97, 5237-5242. doi: 10.1073/pnas.97.10.5237
189. Rasmussen, S., Barah, P., Suarez-Rodriguez, M. C., Bressendorff, S., Friis, P., Costantino, P., et al. (2013). Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 161, 1783-1794. doi: 10.1104/pp.112.210773
190. Rhodes, D., and Hanson, A. D. (1993). Quaternary ammonium and tertiary sulfonium compounds in higher-plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 357-384. doi: 10.1146/ annurev.pp.44.060193.002041
191. Ristic, Z., Wilson, K., Nelsen, C., Mom-cilovic, I., Kobayashi, S., Meeley, R., et al. (2004). A maize mutant with decreased capacity to accumulate chloroplast protein synthesis elongation factor (EF-Tu) displays reduced tolerance to heat stress. Plant Sci. 167, 1367-1374. doi: 10.1016/j. plantsci.2004.07.016
192. Rivero, R. M., Ruiz, J. M., Garcia, P. C., Lopez-Lefebre, L. R., Sanchez, E., and Romero, L. (2001). Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci. 160, 315-321. doi: 10.1016/S0168-9452(00)00395-2
193. Rivero, R. M., Ruiz, J. M., and Romero, L. M. (2004). Importance of N source on heat stress tolerance due to the accumulation of proline and quaternary ammonium compounds in tomato plants. Plant Biol. 6, 702-707. doi: 10.1055/s-2004-821293
194. Rizhsky, L., Liang, H., and Mittler, R. (2002). The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 130, 1143-1151. doi: 10.1104/pp.006858
195. Rizhsky, L., Liang, H. J., Shuman, J., Shulaev, V., Davletova, S., and Mittler, R. (2004). When Defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683-1696. doi: 10.1104/pp.103.033431
196. Ruiz-Ferrer, V., and Voinnet, O. (2009). Roles of plant Small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485-510. doi: 10.1146/ annurev.arplant.043008.092111
197. Rustérucci, C., Espunya, M. C., Diaz, M., Chabannes, M., and Martinez, M. C. (2007). S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol. 143, 1282-1292. doi: 10.1104/pp. 106.091686
198. Saidi, Y., Domini, M., Choy, F., Zryd, J. P., Schwitzguebel, J. P., and Goloubinoff, P. (2007). Activation of the heat shock response in plants by chlorophenols: trans-genic Physcomitrella patens as a sensitive biosensor for organic pollutants. Plant Cell Environ. 30, 753-763. doi: 10.1111/j.1365-3040.2007. 01664.x
199. Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y. G., Maathuis, F. J. M., et al. (2009). The eat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21, 2829-2843. doi: 10.1105/tpc.108.065318
200. Saini, H. S., Sedgley, M., and 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. doi: 10.1071/PP9840243
201. Sairam, R. K., and Tyagi, A. (2004). Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci. 86, 407-421.
202. Sakamoto, A., and Murata, N. (2002). The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25, 163-171. doi: 10.1046/j.0016-8025.2001.00790.x
203. Sakata, T., Oshino, T., Miura, S., Tomabechi, M., Tsunaga, Y., Higashitani, N., et al. (2010). Auxins reverse plant male sterility caused by high temperatures. Proc. Natl. Acad. Sci. U.S.A. 107, 8569-8574. doi: 10.1073/pnas.1000869107
204. Sangwan, V., Orvar, B. L., Beyerly, J., Hirt, H., and Dhindsa, R. S. (2002). Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 31, 629-638. doi: 10.1046/j.1365-313X.2002.01384.x
205. Sano, H., Royer, H. D., and Sager, R. (1980). Identification of 5-methylcytosine in DNA fragments immobilized on nitrocellulose paper. Proc. Natl. Acad. Sci. U.S.A. 77, 3581-3585. doi: 10.1073/pnas.77.6. 3581
206. Sarkar, N. K., Kim, Y. K., and Grover, A. (2009). Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10:393. doi: 10.1186/1471-2164-10-393
207. Sato, S., Kamiyama, M., Iwata, T., Makita, N., Furukawa, H., and Ikeda, H. (2006). Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon escu-lentum by disrupting specific physiological processes in male reproductive development. Ann. Bot. 97, 731-738. doi: 10.1093/aob/mcl037
208. Sato, S., Peet, M. M., and Gardner, R. G. (2004). Altered flower retention and developmental patterns in nine tomato cultivars under elevated temperature. Sci. Hortic. 101, 95-101. doi: 10.1016/j.scienta.2003. 10.008
209. Sato, S., Peet, M. M., and Thomas, J. F. (2002). Determining critical pre- and post-anthesis periods and physiological processes in Lycoper-sicon esculentum Mill. exposed to moderately elevated temperatures. J. Exp. Bot. 53, 1187-1195. doi: 10.1093/jexbot/53.371.1187
210. Sato, S., Tabata, S., Hirakawa, H., Asamizu, E., Shirasawa, K., Isobe, S., et al. (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641. doi: 10.1038/nature11119
211. Savin, R., and Nicolas, M. E. (1996). Effects of short periods of drought and high temperature on grain growth and starch accumulation of two malting barley cultivars. Aust. J. Plant Physiol. 23, 201-210. doi: 10.1071/PP9960201
212. Scharf, K. D., Berberich, T., Ebers-berger, I., and Nover, L. (2012). The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Bio-phys. Acta 1819, 104-119. doi: 10.1016/j.bbagrm.2011.10.002
213. Schijlen, E. G. W. M., De Vos, C. H. R., Martens, S., Jonker, H. H., Rosin, F. M., Molthoff, J. W., et al. (2007). RNA interference silencing of Chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiol. 144, 1520-1530. doi: 10.1104/pp.107.100305
214. Schleiff, E., and Becker, T. (2011). Common ground for protein transloca-tion: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 12, 48-59. doi: 10.1038/nrm3027
215. Schramm, F., Larkindale, J., Kiehlmann, E., Ganguli, A., Englich, G., Vier-ling, E., et al. (2008). A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 53, 264-274. doi: 10.1111/j.1365-313X.2007. 03334.x
216. Schripsema, J. (2010). Application of NMR in plant metabolomics: techniques, problems and prospects. Phytochem. Anal. 21, 14-21. doi: 10.1002/pca.1185
217. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., et al. (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279-292. doi: 10.1046/j.1365-313X.2002.01359.x
218. Sheoran, I. S., Ross, A. R. S., Olson, D. J. H., and Sawhney, V. K. (2007). Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J. Exp. Bot. 58, 3525-3535. doi: 10.1093/jxb/erm199
219. Sidrauski, C., and Walter, P. (1997). The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031-1039. doi: 10.1016/S0092-8674(00) 80369-4
220. Singh, I., and Shono, M. (2005). Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul. 47, 111-119. doi: 10.1007/s10725-005-3252-0
221. Smith, A. P., Jain, A., Deal, R. B., Nagarajan, V. K., Poling, M. D., Raghothama, K. G., et al. (2010). Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol. 152, 217-225. doi: 10.1104/pp.109.145532
222. Song, J. J., Nada, K., and Tachibana, S. (1999). Ameliorative effect of polyamines on the high temperature inhibition of in vitro pollen germination in tomato (Lycopersi-con esculentum Mill.). Sci. Hortic. 80, 203-212. doi: 10.1016/S0304-4238(98)00254-4
223. Song, J. J., Nada, K., and Tachibana, S. (2002). Suppression 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. 43, 619-627. doi: 10.1093/pcp/pcf078
224. Song, S. Q., Lei, Y. B., and Tian, X. R. (2005). Proline metabolism and cross-tolerance to salinity and heat stress in germinating wheat seeds. Russ. J. Plant Physiol. 52, 793-800. doi: 10.1007/s11183-005-0117-3
225. Sugio, A., Dreos, R., Aparicio, F., and Maule, A. J. (2009). The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell 21, 642-654. doi: 10.1105/tpc.108.062596
226. Sunkar, R., Chinnusamy, V., Zhu, J. H., and Zhu, J. K. (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12, 301-309. doi: 10.1016/j.tplants.2007.05.001
227. Sunkar, R., and Zhu, J. K. (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidop-sis. Plant Cell 16, 2001-2019. doi: 10.1105/tpc.104.022830
228. Suzuki, N., Bajad, S., Shuman, J., Shu-laev, V., and Mittler, R. (2008). The transcriptional co-activator MBF1c is a key regulator of thermotoler-ance in Arabidopsis thaliana. J. Biol. Chem. 283, 9269-9275. doi: 10.1074/ jbc.M709187200
229. Suzuki, N., Rizhsky, L., Liang, H. J., Shu-man, J., Shulaev, V., and Mittler, R. (2005). Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coacti-vator multiprotein bridging factor 1c. Plant Physiol. 139, 1313-1322. doi: 10.1104/pp.105.070110
230. Suzuki, N., Sejima, H., Tam, R., Schlauch, K., and Mittler, R. (2011). Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J. 66, 844-851. doi: 10.1111/j.1365-313X.2011.04550.x
231. Szabados, L., and Savouré, A. (2010). Proline: a multifunctional amino acid. Trends Plant Sci. 15, 89-97. doi: 10.1016/j.tplants.2009.11.009
232. Taipale, M., Jarosz, D. F., and Lindquist, S.(2010). HSP90atthehubofprotein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 11, 515-528. doi: 10.1038/nrm2918
233. Takemaru, K., Harashima, S., Ueda, H., and Hirose, S. (1998). Yeast coactivator MBF1 mediates GCN4-dependent transcriptional activation. Mol. Cell. Biol. 18, 4971-4976.
234. Tang, R. S., Zheng, J. C., Jin, Z. Q., Zhang, D., Huang, H., and Chen, L. G. (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. doi: 10.1007/s10725-007-9225-8
235. Taylor, P. E., Glover, J. A., Lavithis, M., Craig, S., Singh, M. B., Knox, R. B., et al. (1998). Genetic control of male fertility in Ara-bidopsis thaliana: structural analyses of postmeiotic developmental mutants. Planta 205, 492-505. doi: 10.1007/s004250050348
236. Tsuda, K., Tsuji, T., Hirose, S., and Yamazaki, K. (2004). Three Ara-bidopsis MBF1 homologs with distinct expression profiles play roles as transcriptional co-activators. Plant Cell Physiol. 45, 225-231. doi: 10.1093/pcp/pch017
237. Tsuda, K., and Yamazaki, K. (2004). Structure and expression analysis of three subtypes of Arabidopsis MBF1 genes. Biochim. Biophys. Acta 1680, 1-10. doi: 10.1016/j.bbaexp. 2004.08.004
238. Tunc-Ozdemir, M., Tang, C., Rahmati, I. M., Brown, E., Groves, N. R., Myers, C. T., et al. (2013). A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol. 161, 1010-1020. doi: 10.1104/pp.112.206888
239. Valluru, R., and Van den Ende, W. (2008). Plant fructans in stress environments: emerging concepts and future prospects. J. Exp. Bot. 59, 2905-2916. doi: 10.1093/jxb/ ern164
240. Vanderauwera, S., Suzuki, N., Miller, G., Van De Cotte, B., Morsa, S., Ravanat, J. L., et al. (2011). Extranuclear protection of chromosomal DNA from oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 108, 1711-1716. doi: 10.1073/pnas.1018359108
241. Vögtle, F. N., and Meisinger, C. (2012). Sensing mitochondrial homeostasis: the protein import machinery takes control. Dev. Cell 23, 674-674. doi: 10.1016/j.devcel. 2012.08.013
242. Wahid, A., and Close, T. J. (2007). Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol. Plant. 51, 104-109. doi: 10.1007/s10535-007-0021-0
243. Wahid, A., Gelani, S., Ashraf, M., and Foolad, M. R. (2007). Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199-223. doi: 10.1016/j.envexpbot.2007.05.011
244. Wahid, A., and Ghazanfar, A. (2006). Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J. Plant Physiol. 163, 723-730. doi: 10.1016/j.jplph. 2005.07.007
245. Wallwork, M. A. B., Jenner, C. F., Logue, S. J., and Sedgley, M. (1998). Effect of high temperature during grain-filling on the structure of developing and malted barley grains. Ann. Bot. 82, 587-599. doi: 10.1006/anbo.1998.0721
246. Wang, X., Cai, J., Liu, F. L., Jin, M., Yu, H. X., Jiang, D., et al. (2012). Pre-anthesis high temperature acclimation alleviates the negative effects of post-anthesis heat stress on stem stored carbohydrates remobilization and grain starch accumulation in wheat. J. Cereal Sci. 55, 331-336. doi: 10.1016/j.jcs.2012.01.004
247. Wang, Z., Gerstein, M., and Sny-der, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63. doi: 10.1038/nrg2484
248. Ward, J. M., Maser, P., and Schroeder, J. I. (2009). Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Phys-iol. 71, 59-82. doi: 10.1146/annurev. physiol.010908.163204
249. Wassenegger, M., Heimes, S., Riedel, L., and Sanger, H. L. (1994). RNA-directed de-novo methylation of genomic sequences in plants. Cell 76, 567-576. doi: 10.1016/0092-8674 (94)90119-8
250. Wei, L. Q., Yan, L. F., and Wang, T. (2011). Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol. 12, R53. doi: 10.1186/gb-2011-12-6-r53
251. Wheeler, T. R., Craufurd, P. Q., Ellis, R. H., Porter, J. R., and Prasad, P. V. V. (2000). Temperature variability and the yield of annual crops. Agric. Ecosyst. Environ. 82, 159-167. doi: 10.1016/S0167-8809(00)00224-3
252. Whittle, C. A., Otto, S. P., Johnston, M. O., and Krochko, J. E. (2009). Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany 87, 650-657. doi: 10.1139/B09-030
253. Windbichler, N., Von Pelchrzim, F., Mayer, O., Csaszar, E., and Schroeder, R. (2008). Isolation of small RNA-binding proteins from E. coli: evidence for frequent interaction of RNAs with RNA poly-merase. RNA Biol. 5, 30-40. doi: 10.4161/rna.5.1.5694
254. Wu, X. L., Shiroto, Y., Kishitani, S., Ito, Y., and Toriyama, K. (2009). Enhanced heat and droughttolerance in transgenic rice seedlings overex-pressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 28, 21-30. doi: 10.1007/s00299-008-0614-x
255. Xin, H. B., Zhang, H., Chen, L., Li, X. X., Lian, Q. L., Yuan, X., et al. (2010a). Cloning and characterization of HsfA2 from Lily (Lilium longi-florum). Plant Cell Rep. 29, 875-885. doi: 10.1007/s00299-010-0873-1
256. Xin, M. M., Wang, Y., Yao, Y. Y., Xie, C. J., Peng, H. R., Ni, Z. F., et al. (2010b). Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aes-tivum L.). BMC Plant Biol. 10:123. doi: 10.1186/1471-2229-10-123
257. Xu, H. W., Lu, Y., Tong, S. Y., and Song, F. B. (2011). Lipid peroxida-tion, antioxidant enzyme activity and osmotic adjustment changes in husk leaves of maize in black soils region of Northeast China. Afr. J. Agric. Res. 6, 3098-3102.
258. Yang, X. H., Liang, Z., and Lu, C. M. (2005). Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol. 138, 2299-2309. doi: 10.1104/pp.105.063164
259. Yang, X. H., Wen, X. G., Gong, H. M., Lu, Q. T., Yang, Z. P., Tang, Y. L., et al. (2007). Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225, 719-733. doi: 10.1007/s00425-006-0380-3
260. Yao, Y. Y., Ni, Z. F., Peng, H. R., Sun, F. L., Xin, M. M., Sunkar, R., et al. (2010). Non-coding small RNAs responsive to abiotic stress in wheat (Triticum aestivum L.). Funct. Integr. Genomics 10, 187-190. doi: 10.1007/s10142-010-0163-6
261. Yoshiba, Y., Kiyosue, T., Katagiri, T., Ueda, H., Mizoguchi, T., Yam-aguchishinozaki, K., et al. (1995). Correlation between the induction of a gene for delta(1)-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis-Thaliana under osmotic-stress. Plant J. 7, 751-760. doi: 10.1046/j.1365-313X.1995.07050751.x
262. Yoshida, T., Ohama, N., Nakajima, J., Kidokoro, S., Mizoi, J., Nakashima, K., et al. (2011). Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol. Genet. Genomics 286, 321-332. doi: 10.1007/s00438-011-0647-7
263. Zanetti, M. E., Blanco, F. A., Daleo, G. R., and Casalongue, C. A. (2003). Phosphorylation of a member of the MBF1 transcriptional co-activator family, StMBF1, is stimulated in potato cell suspensions upon fungal elicitor challenge. J. Exp. Bot. 54, 623-632. doi: 10.1093/jxb/erg061
264. Zhang, H. M., and Zhu, J. K. (2011). RNA-directed DNA methyla-tion. Curr. Opin. Plant Biol 14, 142-147. doi: 10.1016/j.pbi.2011.02.003
265. Zhang, H. Q., and Croes, A. F. (1983). Protection of pollen germination from adverse temperatures -a possible role for Proline. Plant Cell Environ. 6, 471-476. doi: 10.1111/1365-3040.ep11588117
266. Zheng, S. Z., Liu, Y. L., Li, B., Shang, Z. L., Zhou, R. G., and Sun,D.Y. (2012). Phosphoinositide-specific phospho-lipase C9 is involved in the ther-motolerance of Arabidopsis. Plant J. 69, 689-700. doi: 10.1111/j.1365-313X.2011.04823.x
267. Zhu, B. G., Ye, C. J., Lu, H., Chen, X. J., Chai, G., Chen, J. N., et al. (2006). Identification and characterization of a novel heat shock transcription factor gene, GMHsfA1, in soybeans (Glycine max). J. Plant Res. 119, 247-256. doi: 10.1007/s10265-006-0267-1
268. Zinn, K. E., Tunc-Ozdemir, M., and Harper, J. F. (2010). Temperature stress and plant sexual reproduction: uncovering the weakest links. J. Exp. Bot. 61, 1959-1968. doi: 10.1093/jxb/erq053
269. Zou, J. J., Song, L. F., Zhang, W. Z., Wang, Y., Ruan, S. L., and Wu, W. H. (2009). Comparative proteomic analysis of Arabidop-sis mature pollen and germinated pollen. J. Integr. Plant Biol. 51, 438-455. doi: 10.1111/j.1744-7909.2009. 00823.x