Abstract
Key message
Ethylene biosynthesis is regulated in reproductive tissues in response to heat stress in a manner to optimize resource allocation to pollinated fruits with developing seeds.
Abstract
High temperatures during reproductive development are particularly detrimental to crop fruit/seed production. Ethylene plays vital roles in plant development and abiotic stress responses; however, little is known about ethylene’s role in reproductive tissues during development under heat stress. We assessed ethylene biosynthesis and signaling regulation within the reproductive and associated tissues of pea during the developmental phase that sets the stage for fruit-set and seed development under normal and heat-stress conditions. The transcript abundance profiles of PsACS [encode enzymes that convert S-adenosyl-l-methionine to 1-aminocyclopropane-1-carboxylic acid (ACC)] and PsACO (encode enzymes that convert ACC to ethylene), and ethylene evolution were developmentally, environmentally, and tissue-specifically regulated in the floral/fruit/pedicel tissues of pea. Higher transcript abundance of PsACS and PsACO in the ovaries, and PsACO in the pedicels was correlated with higher ethylene evolution and ovary senescence and pedicel abscission in fruits that were not pollinated under control temperature conditions. Under heat-stress conditions, up-regulation of ethylene biosynthesis gene expression in pre-pollinated ovaries was also associated with higher ethylene evolution and lower retention of these fruits. Following successful pollination and ovule fertilization, heat-stress modified PsACS and PsACO transcript profiles in a manner that suppressed ovary ethylene evolution. The normal ethylene burst in the stigma/style and petals following pollination was also suppressed by heat-stress. Transcript abundance profiles of ethylene receptor and signaling-related genes acted as qualitative markers of tissue ethylene signaling events. These data support the hypothesis that ethylene biosynthesis is regulated in reproductive tissues in response to heat stress to modulate resource allocation dynamics.
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References
Abeysingha GLDN (2015) The effect of auxins on seed yield parameters in wheat, pea and canola grown under controlled environment and western canadian field conditions. MSc Thesis, University of Alberta, Edmonton, AB
Aloni B, Karni L, Rylski I (1995) Inhibition of heat induced pepper (Capsicum annuum) flower abscission and induction of fruit malformation by silver thiosulphate. J Hortic Sci Biotech 70:215–220
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18. doi:10.1146/annurev.cellbio.16.1.1
Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086–1089. doi:10.1126/science.241.4869.1086
Brown KM (1997) Ethylene and abscission. Physiol Plant 100:567–576. doi:10.1111/j.1399-3054.1997.tb03062.x
Bueckert RA, Wagenhoffer S, Hnatowich G, Warkentin TD (2015) Effect of heat and precipitation on pea yield and reproductive performance in the field. Can J Plant Sci 95:629–639. doi:10.4141/cjps-2014-342
Bulens I, Van de Poel B, Hertog ML, De Proft MP, Geeraerd AH, Nicolaï BM (2011) Protocol: an updated integrated methodology for analysis of metabolites and enzyme activities of ethylene biosynthesis. Plant Methods 7:17. doi:10.1186/1746-4811-7-17
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144
Cheng M-C, Liao P-M, Kuo W-W, Lin T-P (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582. doi:10.1104/pp.113.221911
DeMartinis D, Mariani C (1999) Silencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants. Plant Cell 11:1061–1072
Dorling SJ, McManus MT (2012) The fate of ACC in higher plants. In: McManus MT Annual plant reviews, vol 44. Wiley, Hoboken, pp 83–115. doi:10.1002/9781118223086.ch4
Druege U (2006) Ethylene and plant responses to abiotic stress. In: Khan NA (ed) Ethylene Action in Plants. Springer, Berlin, pp 81–118. doi:10.1007/978-3-540-32846-9_5
Egli DB, TeKrony DM, Spears JF (2005) Effect of high temperature stress during different stages of seed development in soybean [glycine max (l.) Merrill]. Seed Technol 27:177–189
Foyer CH et al (2016) Neglecting legumes has compromised human health and sustainable food production. Nat Plants 2:16112. doi:10.1038/nplants.2016.112
Gamalero E, Glick BR (2012) Ethylene and abiotic stress tolerance in plants. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 395–412. doi:10.1007/978-1-4614-0815-4
Gross Y, Kigel J (1994) Differential sensitivity to high temperature of stages in the reproductive development of common bean (Phaseolus vulgaris L.). Field Crops Res 36:201–212. doi:10.1016/0378-4290(94)90112-0
Guilioni L, Wery J, Tardieu F (1997) Heat stress-induced abortion of buds and flowers in pea: is sensitivity linked to organ age or to relations between reproductive organs? Ann Bot 80:159–168. doi:10.1006/anbo.1997.0425
Harpaz-Saad S, Yoon GM, Mattoo AK, Kieber JJ (2012) The formation of ACC and competition between polyamines and ethylene for SAM. In: McManus MT Annual plant reviews, vol 44. Wiley, Hoboken, pp 53–81. doi:10.1002/9781118223086.ch3
Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Sci 172:1113–1123. doi:10.1016/j.plantsci.2007.03.004
Hoekstra FA, Weges R (1986) Lack of control by early pistillate ethylene of the accelerated wilting of Petunia hybrida flowers. Plant Physiol 80:403–408
Holden MJ, Marty JA, Singh-Cundy A (2003) Pollination-induced ethylene promotes the early phase of pollen tube growth in Petunia inflata. J Plant Physiol 160:261–269
Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271
Jackson MB (2008) Ethylene-promoted elongation: an adaptation to submergence stress. Ann Bot 101:229–248. doi:10.1093/aob/mcm237
Jayasinghege CPA, Ozga JA, Waduthanthri KD, Reinecke DM (2017) Regulation of ethylene-related gene expression by indole-3-acetic acid and 4-chloroindole-3-acetic acid in relation to pea fruit and seed development. J Exp Bot. doi:10.1093/jxb/erx217
Jeuffroy M, Duthion C, Meynard J, Pigeaire A (1990) Effect of a short period of high day temperatures during flowering on the seed number per pod of pea (Pisum sativum L). Agronomie 10:139–145
Johnstone MMG, Reinecke DM, Ozga JA (2005) The auxins IAA and 4-Cl-IAA differentially modify gibberellin action via ethylene response in developing pea fruit. J Plant Growth Regul 24:214–225. doi:10.1007/s00344-005-0035-9
Jones RA, El-Abd SO (1989) Prevention of salt-induced epinasty by α-aminooxyacetic acid and cobalt. Plant Growth Regul 8:315–323. doi:10.1007/BF00024662
Ju C, Chang C (2015) Mechanistic insights in ethylene perception and signal transduction. Plant Physiol 169:85–95. doi:10.1104/pp.15.00845
Kalantari KM, Smith AR, Hall MA (2000) The effect of water stress on 1-(malonylamino)cyclopropane-1-carboxylic acid concentration in plant tissues. Plant Growth Regul 31:183–193. doi:10.1023/A:1006354415329
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441
Kukreja S, Nandwal AS, Kumar N, Sharma SK, Unvi V, Sharma PK (2005) Plant water status, H2O2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biol Plant 49:305–308. doi:10.1007/s10535-005-5308-4
Lashbrook CC, Tieman DM, Klee HJ (1998) Differential regulation of the tomato ETR gene family throughout plant development. Plant J 15:243–252
Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336. doi:10.1093/jxb/erp204
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Llop-Tous I, Barry CS, Grierson D (2000) Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiol 123:971–978
Lurie S, Handros A, Fallik E, Shapira R (1996) Reversible inhibition of tomato fruit gene expression at high temperature (effects on tomato fruit ripening). Plant Physiol 110:1207–1214. doi:10.1104/pp.110.4.1207
Magnus V, Ozga JA, Reinecke DM, Pierson GL, Larue TA, Cohen JD, Brenner ML (1997) 4-chloroindole-3-acetic and indole-3-acetic acids in Pisum sativum. Phytochemistry 46:675–681. doi:10.1016/S0031-9422(97)00229-X
Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: simple ligand, complex regulation. Curr Opin Plant Biol 16:554–560. doi:10.1016/j.pbi.2013.08.001
Morgan PW, Drew MC (1997) Ethylene and plant responses to stress. Physiol Plant 100:620–630. doi:10.1111/j.1399-3054.1997.tb03068.x
Nadeau CD, Ozga JA, Kurepin LV, Jin A, Pharis RP, Reinecke DM (2011) Tissue-specific regulation of gibberellin biosynthesis in developing pea seeds. Plant Physiol 156:897–912. doi:10.1104/pp.111.172577
O’Neill SD (1997) Pollination regulation of flower development. Annu Rev Plant Physiol Plant Mol Biol 48:547–574. doi:10.1146/annurev.arplant.48.1.547
Oberholster SD, Peterson CM, Dute RR (1991) Pedicel abscission of soybean: cytological and ultrastructural changes induced by auxin and ethephon. Can J Bot 69:2177–2186. doi:10.1139/b91-273
Orzáez D, Blay R, Granell A (1999) Programme of senescence in petals and carpels of Pisum sativum L. flowers and its control by ethylene. Planta 208:220–226
Ozga JA, Brenner ML, Reinecke DM (1992) Seed Effects on Gibberellin Metabolism in Pea Pericarp. Plant Physiol 100:88–94
Ozga JA, Yu J, Reinecke DM (2003) Pollination-, development-, and auxin-specific regulation of gibberellin 3beta-hydroxylase gene expression in pea fruit and seeds. Plant Physiol 131:1137–1146. doi:10.1104/pp.102.015974
Ozga JA, Kaur H, Savada RP, Reinecke DM (2017) Hormonal regulation of reproductive growth under normal and heat-stress conditions in legume and other model crop species. J Exp Bot 68:1885–1894. doi:10.1093/jxb/erw464
Peck SC, Kende H (1998) Differential regulation of genes encoding 1-aminocyclopropane-1-carboxylate (ACC) synthase in etiolated pea seedlings: effects of indole-3-acetic acid, wounding, and ethylene. Plant Mol Biol 38:977–982
Peck SC, Pawlowski K, Kende H (1998) Asymmetric responsiveness to ethylene mediates cell elongation in the apical hook of peas. Plant Cell 10:713
Porch TG, 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
Rieu I, Wolters-Arts M, Derksen J, Mariani C, Weterings K (2003) Ethylene regulates the timing of anther dehiscence in tobacco. Planta 217:131–137. doi:10.1007/s00425-003-0976-9
Rogers HJ (2013) From models to ornamentals: how is flower senescence regulated? Plant Mol Biol 82:563–574. doi:10.1007/s11103-012-9968-0
Sadras VO, Lake L, Chenu K, McMurray LS, Leonforte A (2012) Water and thermal regimes for field pea in Australia and their implications for breeding. Crop Pasture Sci 63:33. doi:10.1071/CP11321
Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714
Steed CL, Harrison MA (1993) Regulation of ethylene biosynthesis after short-term heat treatment in etiolated pea stems. Physiol Plant 87:103–107. doi:10.1111/j.1399-3054.1993.tb08797.x
Tacarindua CRP, Shiraiwa T, Homma K, Kumagai E, Sameshima R (2012) The response of soybean seed growth characteristics to increased temperature under near-field conditions in a temperature gradient chamber. Field Crops Res 131:26–31. doi:10.1016/j.fcr.2012.02.006
Tang X, Woodson WR (1996) Temporal and spatial expression of 1-aminocyclopropane-1-carboxylate oxidase mRNA following pollination of immature and mature petunia flowers. Plant Physiol 112:503–511
Tang X, Gomes A, Bhatia A, Woodson WR (1994) Pistil-specific and ethylene-regulated expression of 1-aminocyclopropane-1-carboxylate oxidase genes in petunia flowers. Plant Cell 6:1227–1239. doi:10.1105/tpc.6.9.1227
Vercher Y, Carbonell J (1991) Changes in the structure of ovary tissues and in the ultrastructure of mesocarp cells during ovary senescence or fruit development induced by plant growth substances in Pisum sativum. Physiol Plant 81:518–527. doi:10.1111/j.1399-3054.1991.tb05094.x
Wang Y, Kumar PP (2007) Characterization of two ethylene receptors PhERS1 and PhETR2 from petunia: PhETR2 regulates timing of anther dehiscence. J Exp Bot 58:533–544. doi:10.1093/jxb/erl229
Wang H et al (2004) Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Mol Biol 55:183–192. doi:10.1007/s11103-004-0113-6
Weller JL, Foo EM, Hecht V, Ridge S, Vander Schoor JK, Reid JB (2015) Ethylene signaling influences light-regulated development in pea. Plant Physiol 169:115–124. doi:10.1104/pp.15.00164
Woltering EJ, Vrije TD, Harren F, Hoekstra FA (1997) Pollination and stigma wounding: same response, different signal? J Exp Bot 48:1027–1033. doi:10.1093/jxb/48.5.1027
Zhao Q, Guo HW (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant 4:626–634. doi:10.1093/mp/ssr042
Acknowledgements
This research was supported by the Natural Sciences and Engineering Research Council of Canada Discovery Grant (138166) to JAO, and grants to JAO and DMR partially funded by Alberta Innovates-BioSolutions (11-005), Alberta Crop Industry Development Fund (11-005), Agriculture & Food Council of Alberta Canadian Agricultural Adaptation Program (AB 1106) and the Alberta Pulse Growers Commission (AB 1106).
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RPS grew and harvested pea tissues, performed all gene expression and ethylene quantitation experiments, and the data analyses for the flower/fruit development and heat stress experiments, provided the initial manuscript draft, and edited subsequent manuscript versions; CPJ provided gene sequences for PsACO2&3, PsETR2, and PsEBF1&2, the primers and probe design for qRT-PCR assays for all genes, performed ACC analysis, and revised final figures; KDW provided technical aid to CPJ; JAO conceived the project and designed all experiments, grew and harvested tissue for ACC analysis; grew plants, performed the experiments, collected data, and analyzed the data for the experiment on the effect of heat stress on reproductive parameters at maturity, interpreted the results of all experiments, and edited and revised the manuscript; DMR conceived the project, interpreted the results, and revised the manuscript and figures.
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Savada, R.P., Ozga, J.A., Jayasinghege, C.P.A. et al. Heat stress differentially modifies ethylene biosynthesis and signaling in pea floral and fruit tissues. Plant Mol Biol 95, 313–331 (2017). https://doi.org/10.1007/s11103-017-0653-1
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DOI: https://doi.org/10.1007/s11103-017-0653-1