Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton

Plant Physiology

Volumn 164, Issue 3, 2014, Pages 1293-1308

  Min, Ling ^a   Li, Yaoyao ^a   Hu, Qin ^a   Zhu, Longfu ^a   Gao, Wenhui ^a   Wu, Yuanlong ^a   Ding, Yuanhao ^a   Liu, Shiming ^a   Yang, Xiyan ^a   Zhang, Xianlong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HISTONE; INDOLEACETIC ACID DERIVATIVE; MESSENGER RNA; SUCROSE; VEGETABLE PROTEIN;

ARTICLE; CARBOHYDRATE METABOLISM; CYTOLOGY; DNA METHYLATION; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GOSSYPIUM; GROWTH, DEVELOPMENT AND AGING; HEAT; KINETICS; METABOLISM; PHYSIOLOGICAL STRESS; PLANT GENOME; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

CARBOHYDRATE METABOLISM; DNA METHYLATION; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; GLUCOSE; GOSSYPIUM; HISTONES; HOT TEMPERATURE; INDOLEACETIC ACIDS; KINETICS; PLANT PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; SUCROSE;

EID: 84897658108     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.232314     Document Type: Article

References (56)

1. Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15: 664-674
2. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447: 407-412
3. Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44: 1627-1629
4. Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130: 1645-1656
5. Deng F, Tu L, Tan J, Li Y, Nie Y, Zhang X (2012) GbPDF1 is involved in cotton fiber initiation via the core cis-element HDZIP2ATATHB2. Plant Physiol 158: 890-904
6. 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
7. 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
8. Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S, Yu P, Breen G, Cohen JD, et al (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108: 20231-20235
9. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5: 1217-1229
10. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420-3435
11. Gray WM, Östin A, Sandberg G, Romano CP, Estelle M (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA 95: 7197-7202
12. Hawker J, Jenner C (1993) High temperature affects the activity of enzymes in the committed pathway of starch synthesis in developing wheat endosperm. Funct Plant Biol 20: 197-209
13. He XJ, Hsu YF, Zhu S, Wierzbicki AT, Pontes O, Pikaard CS, Liu HL, Wang CS, Jin H, Zhu JK (2009) An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4-and RNA-binding protein. Cell 137: 498-508
14. Hedhly A, Hormaza JI, Herrero M (2009) Global warming and sexual plant reproduction. Trends Plant Sci 14: 30-36
15. Henderson IR, Deleris A, Wong W, Zhong X, Chin HG, Horwitz GA, Kelly KA, Pradhan S, Jacobsen SE (2010) The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 6: e1001182
16. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet (Suppl) 33: 245-254
17. Jagadish SV, Craufurd PQ, Wheeler TR (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot 58: 1627-1635
18. Jagadish SV, 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
19. Kleinow T, Bhalerao R, Breuer F, Umeda M, Salchert K, Koncz C (2000) Functional identification of an Arabidopsis snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast. Plant J 23: 115-122
20. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10: 310-316
21. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-220
22. Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16: 19-28
23. Liu H, Li X, Xiao J, Wang S (2012) A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8: 2
24. Liu Y, Koornneef M, Soppe WJ (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19: 433-444
25. Ma J, Wei H, Song M, Pang C, Liu J, Wang L, Zhang J, Fan S, Yu S (2012) Transcriptome profiling analysis reveals that flavonoid and ascorbateglutathione cycle are important during anther development in upland cotton. PLoS ONE 7: e49244
26. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE (2003) DNA methylation-related chromatin remodeling in activitydependent BDNF gene regulation. Science 302: 890-893
27. McClung CR, Davis SJ (2010) Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol 20: R1086-R1092
28. Min L, Zhu L, Tu L, Deng F, Yuan D, Zhang X (2013) Cotton GhCKI disrupts normal male reproduction by delaying tapetum programmed cell death via inactivating starch synthase. Plant J 75: 823-835
29. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37: 118-125
30. Morrissy AS, Morin RD, Delaney A, Zeng T, McDonald H, Jones S, Zhao Y, Hirst M, Marra MA (2009) Next-generation tag sequencing for cancer gene expression profiling. Genome Res 19: 1825-1835
31. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628
32. Nakamura Y, Yuki K, Park SY, Ohya T (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 30: 833-839
33. 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 Cell Physiol 48: 1319-1330
34. Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P (2005) Coldinduced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28: 1534-1551
35. 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
36. Ouyang B, Fei Z, Joung JG, Kolenovsky A, Koh C, Nowak J, Caplan A, Keller WA, Cui Y, Cutler AJ, et al (2012) Transcriptome profiling and methyl homeostasis of an Arabidopsis mutant deficient in S-adenosylhomocysteine hydrolase1 (SAHH1). Plant Mol Biol 79: 315-331
37. Peet M, Sato S, Gardner R (1998) Comparing heat stress effects on malefertile and male-sterile tomatoes. Plant Cell Environ 21: 225-231
38. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709
39. Saini H, Sedgley M, Aspinall D (1984) Development anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Funct Plant Biol 11: 243-253
40. Sairanen I, Novák O, Pěnčík A, Ikeda Y, Jones B, Sandberg G, Ljung K (2012) Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24: 4907-4916
41. 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
42. Sato S, Peet MM, Thomas JF (2002) Determining critical pre-and postanthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures. J Exp Bot 53: 1187-1195
43. Schaffer AA, Petreikov M (1997) Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol 113: 739-746
44. Singh A, Zubko E, Meyer P (2008) Cooperative activity of DNA methyltransferases for maintenance of symmetrical and non-symmetrical cytosine methylation in Arabidopsis thaliana. Plant J 56: 814-823
45. Singh RP, Prasad P, Sunita K, Giri S, Reddy KR (2007) Influence of high temperature and breeding for heat tolerance in cotton: a review. Adv Agron 93: 313-385
46. Stewart JL, Maloof JN, Nemhauser JL (2011) PIF genes mediate the effect of sucrose on seedling growth dynamics. PLoS ONE 6: e19894
47. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
48. Sun J, Qi L, Li Y, Chu J, Li C (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet 8: e1002594
49. 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
50. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35: 259-270
51. Wang K, Wang Z, Li F, Ye W, Wang J, Song G, Yue Z, Cong L, Shang H, Zhu S, et al (2012) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44: 1098-1103
52. Ye R, Wang W, Iki T, Liu C, Wu Y, Ishikawa M, Zhou X, Qi Y (2012) Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol Cell 46: 859-870
53. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57: 508-514
54. Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38: 379-390
55. Zhang Y, Shewry PR, Jones H, Barcelo P, Lazzeri PA, Halford NG (2001) Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J 28: 431-441
56. Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61: 1959-1968