A specific group of genes respond to cold dehydration stress in cut Alstroemeria flowers whereas ambient dehydration stress accelerates developmental senescence expression patterns
Wagstaff, C., Bramke, I., Breeze, E., Thornber, S., Harrison, E., Thomas, B., Buchanan-Wollaston, V., Stead, T. and Rogers, H. (2010) A specific group of genes respond to cold dehydration stress in cut Alstroemeria flowers whereas ambient dehydration stress accelerates developmental senescence expression patterns. Journal of Experimental Botany, 61 (11). pp. 2905-2921. ISSN 0022-0957
To link to this article DOI: 10.1093/jxb/erq113
Petal development and senescence entails a normally irreversible process. It starts with petal expansion and pigment production, and ends with nutrient remobilization and ultimately cell death. In many species this is accompanied by petal abscission. Post-harvest stress is an important factor in limiting petal longevity in cut flowers and accelerates some of the processes of senescence such as petal wilting and abscission. However, some of the effects of moderate stress in young flowers are reversible with appropriate treatments. Transcriptomic studies have shown that distinct gene sets are expressed during petal development and senescence. Despite this, the overlap in gene expression between developmental and stress-induced senescence in petals has not been fully investigated in any species. Here a custom-made cDNA microarray from Alstroemeria petals was used to investigate the overlap in gene expression between developmental changes (bud to first sign of senescence) and typical post-harvest stress treatments. Young flowers were stressed by cold or ambient temperatures without water followed by a recovery and rehydration period. Stressed flowers were still at the bud stage after stress treatments. Microarray analysis showed that ambient dehydration stress accelerates many of the changes in gene expression patterns that would normally occur during developmental senescence. However, a higher proportion of gene expression changes in response to cold stress were specific to this stimulus and not senescence related. The expression of 21 transcription factors was characterized, showing that overlapping sets of regulatory genes are activated during developmental senescence and by different stresses.
Aharoni A, Keizer LCP, Bouwmeester HJ, et al. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. The Plant Cell 2000;12:647-661. Andersen L, Williams MH, Serek M. Reduced water availability improves drought tolerance of potted minature roses: is the ethylene pathway involved? Journal of Horticultural Science and Biotechnology 2004;79:1-13. Andersson A, Keskitalo J, Sjodin A, et al. A transcriptional timetable of autumn senescence. Genome Biology 2004;5:R24. Basset G, Raymond P, Malek L, Brouquisse R. Changes in the expression and the enzymic properties of the 20S proteasome in sugar-starved maize roots. Evidence for an in vivo oxidation of the proteasome. Plant Physiology 2002;128:1149-1162. Breeze E, Wagstaff C, Harrison E, Bramke I, Rogers HJ, Stead AD, Thomas B, Buchanan-Wollaston V. Gene expression patterns to define stages of post-harvest senescence in Alstroemeria petals. Plant Biotechnology Journal 2004;2:155-168. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D. The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnology Journal 2003;1:3-22. Buchanan-Wollaston V, Page T, Harrison E, et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. The Plant Journal 2005;42:567-585. Chanasut U, Rogers HJ, Leverentz MK, Griffiths G, Thomas B, Wagstaff C, Stead AD. Increasing flower longevity in Alstroemeria. Postharvest Biology and Technology 2003;29:325-333. Channelière S, Riviere S, Scalliet G, et al. Analysis of gene expression in rose petals using expressed sequence tags. FEBS Letters 2002;515:35-38. Courtney SE, Rider CC, Stead AD. Changes in protein ubiquitination and the expression of ubiquitin-encoding transcripts in daylily petals during floral development and senescence. Physiologia Plantarum 1994;91:196-204. Doi M, Reid MS. Sucrose improves the postharvest life of cut flowers of a hybrid Limonium. HortScience 1995;30:1058. Dudareva N, Martin D, Kish KM, Kolosova N, Gorenstein N, Fäldt J, Miller B, Bohlmann J. (E)-Ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. The Plant Cell 2003;15:1227-1241. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. The WRKY superfamily of plant transcription factors. Trends in Plant Science 2000;5:199-206. Fang S-C, Fernandez DE. Effect of regulated overexpression of the MADS domain factor AGL15 on flower senescence and fruit maturation. Plant Physiology 2002;130:78-89. Faragher JD, Mayak S, Tirosh T. Physiological response of cut rose flowers to cold storage. Physiologia Plantarum 1986;67:205-210. Ferrante A, Vernieri P, Tognoni F, Serra G. Changes in abscisic acid and flower pigments during floral senescence of petunia. Biologia Plantarum 2006;50:581-585. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 2006;9:436-442. Gibbings JG, Cook BP, Dufault MR, Madden SL, Khuri S, Turnbull CJ, Dunwell JM. Global transcript analysis of rice leaf and seed using SAGE technology. Plant Biotechnology Journal 2003;1:271-285. Gombert J, Etienne P, Ourry A, Le Dily F. The expression patterns of SAG12/Cab genes reveal the spatial and temporal progression of leaf senescence in Brassica napus L. with sensitivity to the environment. Journal of Experimental Botany 2006;57:1949-1956. Guo Y, Cai Z, Gan S. Transcriptome of Arabidopsis leaf senescence. Plant, Cell and Environment 2004;27:521-549. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Research Symposium Series 1999;41:95-98. Hoeberichts FA, van Doorn WG, Vorst O, Hall RD, van Wordragen MF. Sucrose prevents up-regulation of senescence-associated genes in carnation petals. Journal of Experimental Botany 2007;58:2873-2885. Holton TA, Cornish EC. Genetics and biochemistry of anthocyanin biosynthesis. The Plant Cell 1995;7:1071-1083. Hong Y, Wang T-W, Hudak KA, Schade F, Froese CD, Thompson JE. An ethylene-induced cDNA encoding a lipase expressed at the onset of senescence. Proceedings of the National Academy of Sciences, USA 2000;97:8717-8722. Hsiao TC. Plant responses to water stress. Annual Review of Plant Physiology 1973;24:519-570. Huang D, Wu W, Abrams SR, Cutler AJ. The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. Journal of Experimental Botany 2008;59:2991-3007. Jung S-H, Lee J-Y, Lee D-H. Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress. Plant Molecular Biology 2003;52:553-567. Khodakovskaya M, Li Y, Li JS, Vankova R, Malbeck J, McAvoy R. Effects of cor15a-IPT gene expression on leaf senescence in transgenic Petunia×hybrida and Dendranthema×grandiflorum. Journal of Experimental Botany 2005;56:1165-1175. Langston BJ, Bai S, Jones ML. Increases in DNA fragmentation and induction of a senescence-specific nuclease are delayed during corolla senescence in ethylene-insensitive (etr1-1) transgenic petunias. Journal of Experimental Botany 2005;56:15-23. Le Page-Degivry MT, Orlandini M, Garello G, Barthe P, Gudin SJ. Regulation of ABA levels in senescing petals of rose flowers. Plant Growth Regulation 1991;10:6-72. Lee BH, Henderson DA, Zhu JK. The Arabidopsis cold responsive transcriptome and its regulation by ICE1. The Plant Cell 2005;17:3155-3175. Leverentz MK, Wagstaff C, Rogers HJ, Stead AD, Chanasut U, Silkowski H, Thomas B, Weichert H, Feussner I, Griffiths G. Characterization of a novel lipoxygenase-independent senescence mechanism in Alstroemeria peruviana floral tissue. Plant Physiology 2002;130:273-283. Lim PO, Kim HJ, Nam HG. Leaf senescence. Annual Review of Plant Biology 2007;58:115-136. Lin J-F, Wu S-H. Molecular events in senescing Arabidopsis leaves. The Plant Journal 2004;39:612-628. Meyer RC Jr., Goldsbrough PB, Woodson WR. An ethylene-responsive flower senescence-related gene from carnation encodes a protein homologous to glutathione S transferases. Plant Molecular Biology 1991;17:277-281. Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi- Shinozaki K, Matsumoto K, Shinozaki K. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 1996;93:765-769. Moyle R, Fairbairn DJ, Ripi J, Crowe M, Botella JR. Developing pineapple fruit has a small transcriptome dominated by metallothionein. Journal of Experimental Botany 2004;56:101-112. Munne-Bosch S, Alegre L. Die and let live: leaf senescence contributes to plant survival under drought stress. Functional Plant Biology 2004;31:203-216. Nakashima K, Ito Y, Yamaguchi-Shinozaki K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiology 2009;149:88-95. Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K. Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. The Plant Journal 2003;34:868-887. Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K. Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Functional and Integrative Genomics 2006;3:212-234. Panavas T, Walker EL, Rubinstein B. Possible involvement of abscisic acid in senescence of daylily petals. Journal of Experimental Botany 1998;49:1987-1997. Price AM, Aros Orellana DF, Stevens R, Acock R, Buchanan-Wollaston V, Stead AD, Rogers HJ. A comparison of leaf and petal senescence in wallflowers (Erysimum linifolium) reveals common and distinct patterns of gene expression and physiology. Plant Physiology 2008;147:1898-1912. Primack RB. Longevity of individual flowers. Annual Review of Ecology and Systematics 1985;16:15-37. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiology 2003;133:1755-1767. Ranwala AP, Miller WB. Gibberellin(4+7), benzyladenine, and supplemental light improve postharvest leaf and flower quality of cold-stored ‘Stargazer’ hybrid lilies. Journal of the American Society of Horticultural Science 1998;123:563-568. Ranwala AP, Miller WB. Effects of cold storage on post harvest leaf and flower quality of potted Oriental-, Asiatic- and LA-hybrid lily cultivars. Scientia Horticulturae 2005;105:383-392. Reddy AR, Ramakrishna W, Sekhar CA, Nagabhushana I, Babu PR, Bonaldo MF, Soares MB, Bennetzen JL. Novel genes are enriched in normalized cDNA libraries from drought stressed seedlings of rice (Oryza sativa L. subsp. Indica cv. Nagina 22). Genome 2002;45:204-211. Reid M. Produce facts Alstroemeria, Peruvian lily recommendations for maintaining postharvest quality. University of California, Davis: Postharvest Technology Research & Information Center; 2004. Roberts I, Murray PF, Passeron S, Barneix AJ. The activity of the 20S proteasome is maintained in detached wheat leaves during senescence in darkness. Plant Physiology and Biochemistry 2002;40:161-166. Roca M, James C, Pruzinska A, Hortensteiner S, Thomas H, Ougham H. Analysis of the chlorophyll catabolism pathway in leaves of an introgression senescence mutant of. Lolium temulentum. Phytochemistry 2004;65:1231-1238. Rogers HJ. Programmed cell death in floral organs: how and why do flowers die? Annals of Botany 2006;97:309-315. Ross CA, Liu Y, Shen QJ. The WRKY gene family in rice (Oryza sativa). Journal of Integrative Plant Biology 2007;49:827-842. Rudnicki RM, Nowak J, Goszczynska DM. Cold storage and transportation conditions for cut flowers, cuttings and potted plants. Acta Horticulturae 1991;298:225-236. Shinozaki K, Yamaguchi-Shinozaki K, Seki M. Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology 2003;6:410-417. Singh KB, Foley RC, Oñate-Sánchez L. Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 2002;5:430-436. Takahashi S, Seki M, Ishida J, et al. Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Molecular Biology 2004;56:29-55. van der Krol AR, van Poecke RMP, Vorst OFJ, Voogt C, van Leeuwen W, Borst-Vrensen TWM, Takatsuji H, van der Plas LHW. Developmental and wound-, cold-, desiccation-, ultraviolet-B-stress-induced modulations in the expression of the Petunia zinc finger transcription factor gene. ZPT2-21. Plant Physiology 1999;121:1153-1162. van Doorn WG, Balk PA, van Houwelingen AM, Hoeberichts FA, Hall RD, Vorst O, van der Schoot C, van Wordragen MF. Gene expression during anthesis and senescence in Iris flowers. Plant Molecular Biology 2003;53:845-863. van Doorn WG, Woltering EJ. Physiology and molecular biology of petal senescence. Journal of Experimental Botany 2008;59:453-480. Wagstaff C, Chanasut U, Harren FJM, L–J Laarhoven, Thomas B, Rogers HJ Stead AD. Ethylene and flower longevity in Alstroemeria: relationship between tepal senescence, abscission and ethylene biosynthesis. Journal of Experimental Botany 2005;56:1007-1016. Wagstaff C, Leverentz MK, Griffiths G, Thomas B, Chanasut U, Stead AD, Rogers HJ. Protein degradation during senescence of Alstroemeria petals. Journal of Experimental Botany 2002;53:233-240. Wagstaff C, Malcolm P, Rafiq A, Leverentz M, Griffiths G, Thomas B, Stead A, Rogers HJ. Programmed cell death (PCD) processes begin extremely early in Alstroemeria petal senescence. New Phytologist 2003;160:49-59. Search for item at ReadingCrossRefWeb of Science Wagstaff C, Rogers HJ, Leverentz MK, Griffiths G, Thomas B, Chanasut U, Stead AD. Characterisation of Alstroemeria flower vase life. Acta Horticulturae 2001;543:161-175. Wagstaff C, Yang TJW, Stead AD, Buchanan-Wollaston V, Roberts JA. A molecular and structural characterisation of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. The Plant Journal 2009;57:690-705. Weaver LM, Gan S, Quirino B, Amasino RM. A comparison of the expression patterns of several senescence associated genes in response to stress and hormone treatment. Plant Molecular Biology 1998;37:455-469. Zhu J, Dong C-H, Zhu J-K. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Current Opinion in Plant Biology 2007;10:290-295.