An ethylene-induced regulatory module delays flower senescence by regulating cytokinin content

Plant Physiology

Volumn 173, Issue 1, 2017, Pages 853-862

  Wu, Lin ^a   Ma, Nan ^a   Jia, Yangchao ^a   Zhang, Yi ^a   Feng, Ming ^a   Jiang, Cai Zhong ^b,c   Ma, Chao ^d   Gao, Junping ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKININ; ETHYLENE; ETHYLENE DERIVATIVE; PLANT PROTEIN; TRANSCRIPTION FACTOR;

DRUG EFFECTS; FLOWER; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PHYSIOLOGY; ROSE;

CYTOKININS; ETHYLENES; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; PLANT PROTEINS; ROSA; TRANSCRIPTION FACTORS;

EID: 85008721482     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.01064     Document Type: Article

References (58)

1. Agarwal P, Agarwal PK (2014) Pathogenesis related-10 proteins are small, structurally similar but with diverse role in stress signaling. Mol Biol Rep 41: 599-611
2. Ariel F, Diet A, Verdenaud M, Gruber V, Frugier F, Chan R, Crespi M (2010) Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. Plant Cell 22: 2171-2183
3. Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12: 1103-1115
4. Biesiadka J, Bujacz G, Sikorski MM, Jaskolski M (2002) Crystal structures of two homologous pathogenesis-related proteins from yellow lupine. J Mol Biol 319: 1223-1234
5. Chang H, Jones ML, Banowetz GM, Clark DG (2003) Overproduction of cytokinins in petunia flowers transformed with P(SAG12)-IPT delays corolla senescence and decreases sensitivity to ethylene. Plant Physiol 132: 2174-2183
6. Dai F, Zhang C, Jiang X, Kang M, Yin X, Lü P, Zhang X, Zheng Y, Gao J (2012) RhNAC2 and RhEXPA4 are involved in the regulation of dehydration tolerance during the expansion of rose petals. Plant Physiol 160: 2064-2082
7. Eisinger W (1977) Role of cytokinins in carnation flower senescence. Plant Physiol 59: 707-709
8. Fernandes H, Bujacz A, Bujacz G, Jelen F, Jasinski M, Kachlicki P, Otlewski J, Sikorski MM, Jaskolski M (2009) Cytokinin-induced structural adaptability of a Lupinus luteus PR-10 protein. FEBS J 276: 1596-1609
9. Fernandes H, Michalska K, Sikorski M, Jaskolski M (2013) Structural and functional aspects of PR-10 proteins. FEBS J 280: 1169-1199
10. Fernandes H, Pasternak O, Bujacz G, Bujacz A, Sikorski MM, Jaskolski M (2008) Lupinus luteus pathogenesis-related protein as a reservoir for cytokinin. J Mol Biol 378: 1040-1051
11. Gan S, Amasino RM (1997) Making sense of senescence: molecular genetic regulation and manipulation of leaf senescence. Plant Physiol 113: 313-319
12. Hamant O, Nogué F, Belles-Boix E, Jublot D, Grandjean O, Traas J, Pautot V (2002) The KNAT2 homeodomain protein interacts with ethylene and cytokinin signaling. Plant Physiol 130: 657-665
13. Hashimoto M, Kisseleva L, Sawa S, Furukawa T, Komatsu S, Koshiba T (2004) A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol 45: 550-559
14. Henriksson E, Olsson AS, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139: 509-518
15. Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21: 3029-3038
16. Hoeberichts FA, van Doorn WG, Vorst O, Hall RD, van Wordragen MF (2007) Sucrose prevents up-regulation of senescence-associated genes in carnation petals. J Exp Bot 58: 2873-2885
17. Ichimura K, Yamada T, Yoshioka S, Pun U, Tanase K, Shimizu-Yumoto H, Ottosen C, Grout B, Mueller R (2009) Ethylene regulates programmed cell death (PCD) associated with petal senescence in carnation flowers. Acta Hortic 847: 185-190
18. Jones ML, Chaffin GS, Eason JR, Clark DG (2005) Ethylene-sensitivity regulates proteolytic activity and cysteine protease gene expression in petunia corollas. J Exp Bot 56: 2733-2744
19. Lebel S, Schellenbaum P, Walter B, Maillot P (2010) Characterisation of the Vitis vinifera PR10 multigene family. BMC Plant Biol 10: 184
20. Lee SH, Sakuraba Y, Lee T, Kim KW, An G, Lee HY, Paek NC (2015) Mutation of Oryza sativa CORONATINE INSENSITIVE 1b (OsCOI1b) delays leaf senescence. J Integr Plant Biol 57: 562-576
21. Lerslerwong L, Ketsa S, van Doorn WG (2009) Protein degradation and peptidase activity during petal senescence in Dendrobium cv. Khao sanan. Postharvest Biol Technol 52: 84-90
22. Li Z, Peng J, Wen X, Guo H (2013) Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25: 3311-3328
23. Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318: 1302-1305
24. Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 55: 301-310
25. Liu J, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68: 3-13
26. Liu X, Huang B, Lin J, Fei J, Chen Z, Pang Y, Sun X, Tang K (2006) A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress-and pathogen-inducible. J Plant Physiol 163: 546-556
27. Lü P, Zhang C, Liu J, Liu X, Jiang G, Jiang X, Khan MA, Wang L, Hong B, Gao J (2014) RhHB1 mediates the antagonism of gibberellins to ABA and ethylene during rose (Rosa hybrida) petal senescence. Plant J 78: 578-590
28. Lukaszewska AJ, Bianco J, Barthe P, Le Page-Degivry MT (1994) Endogenous cytokinins in rose petals and the effect of exogenously applied cytokinins on flower senescence. Plant Growth Regul 14: 119-126
29. Ma N, Cai L, Lu W, Tan H, Gao J (2005) Exogenous ethylene influences flower opening of cut roses (Rosa hybrida) by regulating the genes encoding ethylene biosynthesis enzymes. Sci China C Life Sci 48: 434-444
30. Ma N, Xue J, Li Y, Liu X, Dai F, Jia W, Luo Y, Gao J (2008) Rh-PIP2;1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiol 148: 894-907
31. Manavella PA, Arce AL, Dezar CA, Bitton F, Renou JP, Crespi M, Chan RL (2006) Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor. Plant J 48: 125-137
32. Mayak S, Halevy AH (1970) Cytokinin activity in rose petals and its relation to senescence. Plant Physiol 46: 497-499
33. Mor Y, Spiegelstein H, Halevy AH (1983) Inhibition of ethylene biosynthesis in carnation petals by cytokinin. Plant Physiol 71: 541-546
34. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5: 986-992
35. Pasternak O, Bujacz GD, Fujimoto Y, Hashimoto Y, Jelen F, Otlewski J, Sikorski MM, Jaskolski M (2006) Crystal structure of Vigna radiata cytokinin-specific binding protein in complex with zeatin. Plant Cell 18: 2622-2634
36. Pei H, Ma N, Tian J, Luo J, Chen J, Li J, Zheng Y, Chen X, Fei Z, Gao J (2013) An NAC transcription factor controls ethylene-regulated cell expansion in flower petals. Plant Physiol 163: 775-791
37. Rogers HJ (2013) From models to ornamentals: How is flower senescence regulated? Plant Mol Biol 82: 563-574
38. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57: 431-449
39. Shahri W, Tahir I (2011) Flower senescence-strategies and some associated events. Bot Rev 77: 152-184
40. Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, Proveniers M, Aalen RB, Butenko MA (2011) Arabidopsis class I KNOTTED-like homeobox proteins act downstream in the IDA-HAE/HSL2 floral abscission signaling pathway. Plant Cell 23: 2553-2567
41. Sikorski MM, Biesiadka J, Kasperska AE, Kopcińnska J, Łotocka B, Golinowski W, Legocki AB (1999) Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules. Plant Sci 149: 125-137
42. Somssich IE, Schmelzer E, Kawalleck P, Hahlbrock K (1988) Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Mol Gen Genet 213: 93-98
43. Srivastava S, Emery RN, Kurepin LV, Reid DM, Fristensky B, Kav NN (2006) Pea PR 10.1 is a ribonuclease and its transgenic expression elevates cytokinin levels. Plant Growth Regul 49: 17-25
44. Srivastava S, Emery RN, Rahman MH, Kav NN (2007) A crucial role for cytokinins in pea ABR17-mediated enhanced germination and early seedling growth of Arabidopsis thaliana under saline and low-temperature stresses. J Plant Growth Regul 26: 26-37
45. Taverner E, Letham DS, Wang J, Cornish E, Willcocks DA (1999) Influence of ethylene on cytokinin metabolism in relation to Petunia corolla. Phytochemistry 51: 341-347
46. Tian J, Pei H, Zhang S, Chen J, Chen W, Yang R, Meng Y, You J, Gao J, Ma N (2014) TRV-GFP: a modified Tobacco rattle virus vector for efficient and visualizable analysis of gene function. J Exp Bot 65: 311-322
47. Tripathi SK, Tuteja N (2007) Integrated signaling in flower senescence: an overview. Plant Signal Behav 2: 437-445
48. van Doorn WG (2001) Categories of petal senescence and abscission: a re-evaluation. Ann Bot (Lond) 87: 447-456
49. van Doorn WG, Woltering EJ (2008) Physiology and molecular biology of petal senescence. J Exp Bot 59: 453-480
50. van Staden J, Upfold SJ, Bayley AD, Drewes FE (1990) Cytokinin in cut carnation flower. IX. Transport and metabolism of iso-pentenyladenine and the effect of its derivatives on flower longevity. Plant Growth Regul 9: 255-261
51. Wagstaff C, Leverentz MK, Griffiths G, Thomas B, Chanasut U, Stead AD, Rogers HJ (2002) Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals. J Exp Bot 53: 233-240
52. Walter MH, Liu JW, Wünn J, Hess D (1996) Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental, dark-induced and exogenous-stimulus-dependent expression. Eur J Biochem 239: 281-293
53. Xu TF, Zhao XC, Jiao YT, Wei JY, Wang L, Xu Y (2014) A pathogenesis related protein, VpPR-10.1, from Vitis pseudoreticulata: an insight of its mode of antifungal activity. PLoS One 9: e95102
54. Xu Y, Ishida H, Reisen D, Hanson MR (2006) Upregulation of a tonoplast-localized cytochrome P450 during petal senescence in Petunia inflata. BMC Plant Biol 6: 8
55. Xue J, Li Y, Tan H, Yang F, Ma N, Gao J (2008) Expression of ethylene biosynthetic and receptor genes in rose floral tissues during ethylene-enhanced flower opening. J Exp Bot 59: 2161-2169
56. Yamada T, Ichimura K, Kanekatsu M, van Doorn WG (2009) Homologs of genes associated with programmed cell death in animal cells are differentially expressed during senescence of Ipomoea nil petals. Plant Cell Physiol 50: 610-625
57. Zhang H, Zhou C (2013) Signal transduction in leaf senescence. Plant Mol Biol 82: 539-545
58. Zubini P, Zambelli B, Musiani F, Ciurli S, Bertolini P, Baraldi E (2009) The RNA hydrolysis and the cytokinin binding activities of PR-10 proteins are differently performed by two isoforms of the Pru p 1 peach major allergen and are possibly functionally related. Plant Physiol 150: 1235-1247