Balancing of hormonal biosynthesis and catabolism pathways, a strategy to ameliorate the negative effects of heat stress on reproductive growth.
Abscisic Acid
/ metabolism
Ethylenes
/ biosynthesis
Flowers
/ physiology
Fruit
/ growth & development
Gene Expression Profiling
Gene Expression Regulation, Plant
Gibberellins
/ metabolism
Heat-Shock Response
/ physiology
Indoleacetic Acids
/ metabolism
Metabolomics
Models, Biological
Pisum sativum
/ growth & development
Plant Growth Regulators
/ biosynthesis
Seeds
/ physiology
Up-Regulation
/ genetics
Pisum sativum
abscisic acid
auxin
ethylene
gene expression
gibberellin
heat stress
hormone biosynthesis and catabolism
seed and fruit development
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
received:
07
11
2019
accepted:
29
05
2020
pubmed:
10
6
2020
medline:
2
9
2021
entrez:
10
6
2020
Statut:
ppublish
Résumé
In pea (Pisum sativum L.), moderate heat stress during early flowering/fruit set increased seed/ovule abortion, and concomitantly produced fruits with reduced ovary (pericarp) length, and fewer seeds at maturity. Plant hormonal networks coordinate seed and pericarp growth and development. To determine if these hormonal networks are modulated in response to heat stress, we analyzed the gene expression patterns and associated these patterns with precursors, and bioactive and inactive metabolites of the auxin, gibberellin (GA), abscisic acid (ABA), and ethylene biosynthesis/catabolism pathways in young developing seeds and pericarps of non-stressed and 4-day heat-stressed fruits. Our data suggest that within the developing seeds heat stress decreased bioactive GA levels reducing GA growth-related processes, and that increased ethylene levels may have promoted this inhibitory response. In contrast, heat stress increased auxin biosynthesis gene expression and auxin levels in the seeds and pericarps, and seed ABA levels, both effects can increase seed sink strength. We hypothesize that seeds with higher auxin- and ABA-induced sink strength and adequate bioactive GA levels will set and continue to grow, while the seeds with lower sink strength (low auxin, ABA, and GA levels) will become more sensitive to heat stress-induced ethylene leading to ovule/seed abortion.
Substances chimiques
Ethylenes
0
Gibberellins
0
Indoleacetic Acids
0
Plant Growth Regulators
0
Abscisic Acid
72S9A8J5GW
ethylene
91GW059KN7
gibberellic acid
BU0A7MWB6L
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1486-1503Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Abeysingha G. L. D. N. (2015). The effects of auxins on seed yield parameters in wheat, pea and canola grown under controlled environmental and Western Canadian field conditions. M.Sc. thesis, University of Alberta. https://doi.org/10.7939/R38K75492
Abhinandan, K., Skori, L., Stanic, M., Hickerson, N. M. N., Jamshed, M., & Samuel, M. A. (2018). Abiotic stress signaling in wheat - An inclusive overview of hormonal interactions during abiotic stress responses in wheat. Frontiers in Plant Science, 9, 734-734. https://doi.org/10.3389/fpls.2018.00734
Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., & Genschik, P. (2008). The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell, 20(8), 2117-2129. https://doi.org/10.1105/tpc.108.058941
Bennett, E. J., Roberts, J. A., & Wagstaff, C. (2011). The role of the pod in seed development: Strategies for manipulating yield. New Phytologist, 190(4), 838-853. https://doi.org/10.1111/j.1469-8137.2011.03714.x
Browning, G. (1980). Endogenous cis,trans-abscisic acid and pea seed development: Evidence for a role in seed growth from changes induced by temperature. Journal of Experimental Botany, 31(120), 185-197.
Bueckert, R. A., Wagenhoffer, S., Hnatowich, G., & Warkentin, T. D. (2015). Effect of heat and precipitation on pea yield and reproductive performance in the field. Canadian Journal of Plant Science, 95(4), 629-639. https://doi.org/10.4141/cjps-2014-342
Carbonell-Bejerano, P., Urbez, C., Granell, A., Carbonell, J., & Perez-Amador, M. A. (2011). Ethylene is involved in pistil fate by modulating the onset of ovule senescence and the GA-mediated fruit set in Arabidopsis. BMC Plant Biology, 11, 84. https://doi.org/10.1186/1471-2229-11-84
Carra, B., Pasa, M. S., da Silva, C. P., do Amarante, C. V. T., Steffens, C. A., Bartnicki, V. A., … Einhorn, T. (2018). Early spring inhibition of ethylene synthesis increases fruit set and yield of 'Rocha' pear trees in southern Brazil. Scientia Horticulturae, 232, 92-96. https://doi.org/10.1016/j.scienta.2017.12.062.
Cheng, W.-H., Endo, A., Zhou, L., Penney, J., Chen, H.-C., Arroyo, A., … Sheen, J. (2002). A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. The Plant Cell, 14(11), 2723-2743. https://doi.org/10.1105/tpc.006494.
Colebrook, E. H., Thomas, S. G., Phillips, A. L., & Hedden, P. (2014). The role of gibberellin signalling in plant responses to abiotic stress. The Journal of Experimental Biology, 217(1), 67-75. https://doi.org/10.1242/jeb.089938
Cooper, D. C. (1938). Embryology of Pisum sativum. Botanical Gazette, 100(1), 123-132. https://doi.org/10.1086/334769
Cutler, A., & Krochko, J. (2000). Formation and breakdown of ABA. Trends in Plant Science, 4, 472-478. https://doi.org/10.1016/S1360-1385(99)01497-1
Davidson, S. E., Smith, J. J., Helliwell, C. A., Poole, A. T., & Reid, J. B. (2004). The pea gene LH encodes ent-kaurene oxidase. Plant Physiology, 134(3), 1123-1134. https://doi.org/10.1104/pp.103.032706
Davière, J.-M., & Achard, P. (2016). A pivotal role of DELLAs in regulating multiple hormone signals. Molecular Plant, 9(1), 10-20. https://doi.org/10.1016/j.molp.2015.09.011
Dolferus, R., Ji, X., & Richards, R. A. (2011). Abiotic stress and control of grain number in cereals. Plant Science, 181(4), 331-341. https://doi.org/10.1016/j.plantsci.2011.05.015
Dorcey, E., Urbez, C., Blázquez, M. A., Carbonell, J., & Perez-Amador, M. A. (2009). Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. The Plant Journal, 58(2), 318-332. https://doi.org/10.1111/j.1365-313X.2008.03781.x
Eeuwens, C. J., & Schwabe, W. W. (1975). Seed and pod wall development in Pisum sativum L. in relation to extracted and applied hormones. Journal of Experimental Botany, 26(1), 1-14. https://doi.org/10.1093/jxb/26.1.1
Endo, A., Okamoto, M., & Koshiba, T. (2014). ABA biosynthetic and catabolic pathways. In D.- P. Zhang (Ed.), Abscisic acid: Metabolism, transport and signaling (pp. 21-45). Dordrecht, the Netherlands: Springer. https://doi.org/10.1007/978-94-017-9424-4_2
Feng, J., Dai, C., Luo, H., Han, Y., Liu, Z., & Kang, C. (2019). Reporter gene expression reveals precise auxin synthesis sites during fruit and root development in wild strawberry. Journal of Experimental Botany, 70(2), 563-574. https://doi.org/10.1093/jxb/ery384
Figueiredo, D. D., Batista, R. A., Roszak, P. J., Hennig, L., & Köhler, C. (2016). Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife, 5, e20542. https://doi.org/10.7554/eLife.20542
Figueiredo, D. D., & Köhler, C. (2018). Auxin: A molecular trigger of seed development. Genes & Development, 32(7-8), 479-490. https://doi.org/10.1101/gad.312546.118
Finkelstein, R. R. (2010). The role of hormones during seed development and germination. In P. J. Davies (Ed.), Plant hormones: Biosynthesis, signal transduction, action! (pp. 549-573). Dordrecht, the Netherlands: Springer. https://doi.org/10.1007/978-1-4020-2686-7
Finkelstein, R. R., Gampala, S. S. L., & Rock, C. D. (2002). Abscisic acid signaling in seeds and seedlings. The Plant Cell, 14, S15-S45. https://doi.org/10.1105/tpc.010441
Frey, A., Godin, B., Bonnet, M., Sotta, B., & Marion-Poll, A. (2004). Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta, 218(6), 958-964. https://doi.org/10.1007/s00425-003-1180-7
Garcia-Martinez, J. L., & Carbonell, J. (1980). Fruit-set of unpollinated ovaries of Pisum sativum L.: Influence of plant-growth regulators. Planta, 147(5), 451-456. https://doi.org/10.1007/bf00380187
Garcia-Martinez, J. L., López-Díaz, I., Sánchez-Beltrán, M. J., Phillips, A. L., Ward, D. A., Gaskin, P., & Hedden, P. (1997). Isolation and transcript analysis of gibberellin 20-oxidase genes in pea and bean in relation to fruit development. Plant Molecular Biology, 33, 1073-1084. https://doi.org/10.1023/a:1005715722193
García-Martinez, J. L., Santes, C., Croker, S. J., & Hedden, P. (1991). Identification, quantitation and distribution of gibberellins in fruits of Pisum sativum L. cv. Alaska during pod development. Planta, 184(1), 53-60. https://doi.org/10.1007/bf00208236
George, D., & Mallery, P. (2018). IBM SPSS Statistics 25 Step by Step: A Simple Guide and Reference, 15th Edition. USA: Routledge. https://routledgetextbooks.com/textbooks /97811338491076
Gillaspy, G., Ben-David, H., & Gruissem, W. (1993). Fruits: A developmental perspective. The Plant Cell, 5(10), 1439-1451. https://doi.org/10.1105/tpc.5.10.1439
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? Annals of Botany, 80(2), 159-168. https://doi.org/10.1006/anbo.1997.0425
Hays, D. B., Do, J. H., Mason, R. E., Morgan, G., & Finlayson, S. A. (2007). Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Science, 172(6), 1113-1123. https://doi.org/10.1016/j.plantsci.2007.03.004
Hedden, P., & Phillips, A. L. (2000). Gibberellin metabolism: New insights revealed by the genes. Trends in Plant Science, 5(12), 523-530. https://doi.org/10.1016/S1360-1385(00)01790-8
Hedden, P., & Thomas, S. G. (2012). Gibberellin biosynthesis and its regulation. Biochemical Journal, 444(1), 11-25. https://doi.org/10.1042/bj20120245
Hedhly, A., Hormaza, J. I., & Herrero, M. (2009). Global warming and sexual plant reproduction. Trends in Plant Science, 14(1), 30-36. https://doi.org/10.1016/j.tplants.2008.11.001
Jagadish, S., Craufurd, P., & Wheeler, T. (2007). High temperature stress and spikelet fertility in rice (Oryza sativa L.). Journal of Experimental Botany, 58(7), 1635-1627. https://doi.org/10.1093/jxb/erm003
Jayasinghege, C. P. A., Ozga, J. A., Nadeau, C. D., Kaur, H., & Reinecke, D. M. (2019). TIR1 auxin receptors are implicated in the differential response to 4-Cl-IAA and IAA in developing pea fruit. Journal of Experimental Botany, 70(4), 1239-1253. https://doi.org/10.1093/jxb/ery456
Jayasinghege, C. P. A., Ozga, J. A., Waduthanthri, K. D., & Reinecke, D. M. (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. Journal of Experimental Botany, 68(15), 4137-4151. https://doi.org/10.1093/jxb/erx217
Jiang, Y., Davis, A. R., Vujanovic, V., & Bueckert, R. A. (2019). Reproductive development response to high daytime temperature in field pea. Journal of Agronomy and Crop Science, 205(3), 324-333. https://doi.org/10.1111/jac.12328
Jiang, Y., Lahlali, R., Karunakaran, C., Kumar, S., Davis, A. R., & Bueckert, R. A. (2015). Seed set, pollen morphology and pollen surface composition response to heat stress in field pea. Plant, Cell & Environment, 38(11), 2387-2397. https://doi.org/10.1111/pce.12589
Jiang, Y., Lahlali, R., Karunakaran, C., Warkentin, T. D., Davis, A. R., & Bueckert, R. A. (2019). Pollen, ovules, and pollination in pea: Success, failure, and resilience in heat. Plant, Cell & Environment, 42(1), 354-372. https://doi.org/10.1111/pce.13427
Johnstone, M. M. G., Reinecke, D. M., & Ozga, J. A. (2005). The auxins IAA and 4-Cl-IAA differentially modify gibberellin action via ethylene response in developing pea fruit. Journal of Plant Growth Regulation, 24(3), 214-225. https://doi.org/10.1007/s00344-005-0035-9
Kanno, Y., Jikumaru, Y., Hanada, A., Nambara, E., Abrams, S. R., Kamiya, Y., & Seo, M. (2010). Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant and Cell Physiology, 51(12), 1988-2001. https://doi.org/10.1093/pcp/pcq158
Kreplak, J., Madoui, M.-A., Cápal, P., Novák, P., Labadie, K., Aubert, G., … Burstin, J. (2019). A reference genome for pea provides insight into legume genome evolution. Nature Genetics, 51(9), 1411-1422. https://doi.org/10.1038/s41588-019-0480-1
Lambert, R. G., & Linck, A. J. (1958). Effects of high temperature on yield of peas. Plant Physiology, 33(5), 347-350. https://doi.org/10.1104/pp.33.5.347
Larsson, E., Vivian-Smith, A., Offringa, R., & Sundberg, E. (2017). Auxin homeostasis in Arabidopsis ovules is anther-dependent at maturation and changes dynamically upon fertilization. Frontiers in Plant Science, 8, 1735. https://doi.org/10.3389/fpls.2017.01735
Lester, D. R., Ross, J. J., Ait-Ali, T., Martin, D. N., & Reid, J. B. (1996). A gibberellin 20-oxidase cDNA (accession no. U58830) from pea seed (PGR 96-050). Plant Physiology, 111, 1353-1354.
Lester, D. R., Ross, J. J., Davies, P. J., & Reid, J. B. (1997). Mendel's stem length gene (Le) encodes a gibberellin 3 beta-hydroxylase. The Plant Cell, 9(8), 1435-1443. https://doi.org/10.1105/tpc.9.8.1435
Lester, D. R., Ross, J. J., Smith, J. J., Elliott, R. C., & Reid, J. B. (1999). Gibberellin 2-oxidation and the SLN gene of Pisum sativum. The Plant Journal, 19(1), 65-73. https://doi.org/10.1046/j.1365-313X.1999.00501.x
Lin, Z., Zhong, S., & Grierson, D. (2009). Recent advances in ethylene research. Journal of Experimental Botany, 60(12), 3311-3336. https://doi.org/10.1093/jxb/erp204
Liu, Y., Li, J., Zhu, Y., Jones, A., Rose, R. J., & Song, Y. (2019). Heat stress in legume seed setting: Effects, causes, and future prospects. Frontiers in Plant Science, 10, 938. https://doi.org/10.3389/fpls.2019.00938
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402-408. https://doi.org/10.1006/meth.2001.1262
Magnus, V., Ozga, J. A., Reinecke, D. M., Pierson, G. L., Larue, T. A., Cohen, J. D., & Brenner, M. L. (1997). 4-chloroindole-3-acetic and indole-3-acetic acids in Pisum sativum. Phytochemistry, 46(4), 675-681. https://doi.org/10.1016/S0031-9422(97)00229-X
Marinos, N. G. (1970). Embryogenesis of the pea (Pisum sativum) I. The cytological environment of the developing embryo. Protoplasma, 70(3), 261-279. https://doi.org/10.1007/bf01275757
Martin, D. N., Proebsting, W. M., & Hedden, P. (1997). Mendel's dwarfing gene: cDNAs from the Le alleles and function of the expressed proteins. Proceedings of the National Academy of Sciences of the United States of America, 94(16), 8907-8911. https://doi.org/10.1073/pnas.94.16.8907
Martin, D. N., Proebsting, W. M., & Hedden, P. (1999). The SLENDER gene of pea encodes a gibberellin 2-oxidase. Plant Physiology, 121(3), 775-781. https://doi.org/10.1104/pp.121.3
Martínez, C., Manzano, S., Megías, Z., Garrido, D., Picó, B., & Jamilena, M. (2013). Involvement of ethylene biosynthesis and signalling in fruit set and early fruit development in zucchini squash (Cucurbita pepo L.). BMC Plant Biology, 13, 139. https://doi.org/10.1186/1471-2229-13-139
Moore-Gordon, C. S., Cowan, A. K., Bertling, I., Botha, C. E. J., & Cross, R. H. M. (1998). Symplastic solute transport and avocado fruit development: A decline in cytokinin/ABA ratio is related to appearance of the hass small fruit variant. Plant and Cell Physiology, 39(10), 1027-1038. https://doi.org/10.1093/oxfordjournals.pcp.a029299
Müntz, K., Rudolph, A., Schlesier, G., & Silhengst, P. (1978). The function of the pericarp in fruits of crop legumes. Die Kulturpflanze, 26(1), 37-67. https://doi.org/10.1007/bf02017331
Nadeau, C. D., Ozga, J. A., Kurepin, L. V., Jin, A., Pharis, R. P., & Reinecke, D. M. (2011). Tissue-specific regulation of gibberellin biosynthesis in developing pea seeds. Plant Physiology, 156(2), 897-912. https://doi.org/10.1104/pp.111.172577
Nambara, E., & Marion-Poll, A. (2005). Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology, 56(1), 165-185. https://doi.org/10.1146/annurev.arplant.56.032604.144046
Nitsch, J. P. (1952). Plant hormones in the development of fruits. The Quarterly Review of Biology, 27(1), 33-57.
Nuttall, J. G., Barlow, K. M., Delahunty, A. J., Christy, B. P., & O'Leary, G. J. (2018). Acute high temperature response in wheat. Agronomy Journal, 110(4), 1296-1308. https://doi.org/10.2134/agronj2017.07.0392
Ofir, M., Gross, Y., Bangerth, F., & Kigel, J. (1993). High temperature effects on pod and seed production as related to hormone levels and abscission of reproductive structures in common bean (Phaseolus vulgaris L.). Scientia Horticulturae, 55(3), 201-211. https://doi.org/10.1016/0304-4238(93)90032-L
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(2), 220-226. https://doi.org/10.1007/s004250050553
Ozga, J. A., Brenner, M. L., & Reinecke, D. M. (1992). Seed effects on gibberellin metabolism in pea pericarp. Plant Physiology, 100(1), 88-94. https://doi.org/10.1104/pp.100.1.88
Ozga, J. A., Kaur, H., Savada, R. P., & Reinecke, D. M. (2017). Hormonal regulation of reproductive growth under normal and heat-stress conditions in legume and other model crop species. Journal of Experimental Botany, 68(8), 1885-1894. https://doi.org/10.1093/jxb/erw464
Ozga, J. A., & Reinecke, D. M. (2003). Hormonal interactions in fruit development. Journal of Plant Growth Regulation, 22(1), 73-81. https://doi.org/10.1007/s00344-003-0024-9
Ozga, J. A., Reinecke, D. M., Ayele, B. T., Ngo, P., Nadeau, C., & Wickramarathna, A. D. (2009). Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit. Plant Physiology, 150(1), 448-462. https://doi.org/10.1104/pp.108.132027
Ozga, J. A., van Huizen, R., & Reinecke, D. M. (2002). Hormone and seed-specific regulation of pea fruit growth. Plant Physiology, 128(4), 1379-1389. https://doi.org/10.1104/pp.010800
Ozga, J. A., Yu, J., & Reinecke, D. M. (2003). Pollination-, development-, and auxin-specific regulation of gibberellin 3β-hydroxylase gene expression in pea fruit and seeds. Plant Physiology, 131(3), 1137-1146. https://doi.org/10.1104/pp.102.015974
Pattison, R. J., & Catalá, C. (2012). Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/LAX gene families. The Plant Journal, 70(4), 585-598. https://doi.org/10.1111/j.1365-313X.2011.04895.x
Puteh, A., Thuzar, M., Mondal, M., Abdullah, N. P. B., & Halim, M. (2013). Soybean [Glycine max (L.) Merrill] seed yield response to high temperature stress during reproductive growth stages. Australian Journal of Crop Science, 7(10), 1472-1479.
Radchuk, R., Conrad, U., Saalbach, I., Giersberg, M., Emery, R. J. N., Küster, H., … Weber, H. (2010). Abscisic acid deficiency of developing pea embryos achieved by immunomodulation attenuates developmental phase transition and storage metabolism. The Plant Journal, 64(5), 715-730. https://doi.org/10.1111/j.1365-313X.2010.04376.x
Reinecke, D. M. (1999). 4-Chloroindole-3-acetic acid and plant growth. Plant Growth Regulation, 27(1), 3-13. https://doi.org/10.1023/a:1006191917753
Reinecke, D. M., Ozga, J. A., & Magnus, V. (1995). Effect of halogen substitution of indole-3-acetic acid on biological activity in pea fruit. Phytochemistry, 40(5), 1361-1366. https://doi.org/10.1016/0031-9422(95)00367-G
Reinecke, D. M., Wickramarathna, A. D., Ozga, J. A., Kurepin, L. V., Jin, A. L., Good, A. G., & Pharis, R. P. (2013). Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiology, 163(2), 929-945. https://doi.org/10.1104/pp.113.225987
Robert, H. S., Park, C., Gutièrrez, C. L., Wójcikowska, B., Pěnčík, A., Novák, O., … Laux, T. (2018). Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nature Plants, 4(8), 548-553. https://doi.org/10.1038/s41477-018-0204-z
Rock, C. D., Heath, T. G., Gage, D. A., & Zeevaart, J. A. D. (1991). Abscisic alcohol is an intermediate in abscisic acid biosynthesis in a shunt pathway from abscisic aldehyde. Plant Physiology, 97(2), 670-676. https://doi.org/10.1104/pp.97.2.670
Rodrigo, M. J., García-Martínez, J. L., Santes, C. M., Gaskin, P., & Hedden, P. (1997). The role of gibberellins A1 and A3 in fruit growth of Pisum sativum L. and the identification of gibberellins A4 and A7 in young seeds. Planta, 201(4), 446-455. https://doi.org/10.1007/s004250050088
Roeder, A. H. K., & Yanofsky, M. F. (2006). Fruit development in Arabidopsis. In C. R. Somerville & E. M. Meyerowitz (Eds.), The Arabidopsis book (Vol. 4, e0075). Rockville, MD: American Society of Plant Biologists. https://doi.org/10.1199/tab.0075
Sakata, T., Oshino, T., Miura, S., Tomabechi, M., Tsunaga, Y., Higashitani, N., … Higashitani, A. (2010). Auxins reverse plant male sterility caused by high temperatures. Proceedings of the National Academy of Sciences of the United States of America, 107(19), 8569-8574. https://doi.org/10.1073/pnas.1000869107
Savada, R. P., Ozga, J. A., Jayasinghege, C. P. A., Waduthanthri, K. D., & Reinecke, D. M. (2017). Heat stress differentially modifies ethylene biosynthesis and signaling in pea floral and fruit tissues. Plant Molecular Biology, 95(3), 313-331. https://doi.org/10.1007/s11103-017-0653-1
Sawicki, M., Aït Barka, E., Clément, C., Vaillant-Gaveau, N., & Jacquard, C. (2015). Cross-talk between environmental stresses and plant metabolism during reproductive organ abscission. Journal of Experimental Botany, 66(7), 1707-1719. https://doi.org/10.1093/jxb/eru533
Serrani, J. C., Ruiz-Rivero, O., Fos, M., & García-Martínez, J. L. (2008). Auxin-induced fruit-set in tomato is mediated in part by gibberellins. The Plant Journal, 56(6), 922-934. https://doi.org/10.1111/j.1365-313X.2008.03654.x
Serrani, J. C., Sanjuán, R., Ruiz-Rivero, O., Fos, M., & García-Martínez, J. L. (2007). Gibberellin regulation of fruit set and growth in tomato. Plant Physiology, 145(1), 246-257. https://doi.org/10.1104/pp.107.098335
Shinozaki, Y., Ezura, H., & Ariizumi, T. (2018). The role of ethylene in the regulation of ovary senescence and fruit set in tomato (Solanum lycopersicum). Plant Signaling & Behavior, 13(4), e1146844. https://doi.org/10.1080/15592324.2016.1146844
Shinozaki, Y., Hao, S., Kojima, M., Sakakibara, H., Ozeki-Iida, Y., Zheng, Y., … Ariizumi, T. (2015). Ethylene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism. The Plant Journal, 83(2), 237-251. https://doi.org/10.1111/tpj.12882
Sita, K., Sehgal, A., HanumanthaRao, B., Nair, R. M., Vara Prasad, P. V., Kumar, S., … Nayyar, H. (2017). Food legumes and rising temperatures: Effects, adaptive functional mechanisms specific to reproductive growth stage and strategies to improve heat tolerance. Frontiers in Plant Science, 8, 1658. https://doi.org/10.3389/fpls.2017.01658
Smit, M. E., & Weijers, D. (2015). The role of auxin signaling in early embryo pattern formation. Current Opinion in Plant Biology, 28, 99-105. https://doi.org/10.1016/j.pbi.2015.10.001
Stanfield, B., Ormrod, D. P., & Fletcher, H. F. (1966). Response of peas to environment: II. Effects of temperature in controlled-environment cabinets. Canadian Journal of Plant Science, 46(2), 195-203. https://doi.org/10.4141/cjps66-029
Swain, S. M., Reid, J. B., & Kamiya, Y. (1997). Gibberellins are required for embryo growth and seed development in pea. The Plant Journal, 12(6), 1329-1338. https://doi.org/10.1046/j.1365-313x.1997.12061329.x
Swain, S. M., Reid, J. B., & Ross, J. J. (1993). Seed development in Pisum. Planta, 191(4), 482-488. https://doi.org/10.1007/bf00195749
Swain, S. M., Ross, J. J., Reid, J. B., & Kamiya, Y. (1995). Gibberellins and pea seed development: Expression of the lhi, ls and le5839 mutations. Planta, 195(3), 426-433. https://doi.org/10.1007/bf00202601
Tivendale, N. D., Davidson, S. E., Davies, N. W., Smith, J. A., Dalmais, M., Bendahmane, A. I., … Ross, J. J. (2012). Biosynthesis of the halogenated auxin, 4-chloroindole-3-acetic acid. Plant Physiology, 159(3), 1055-1063. https://doi.org/10.1104/pp.112.198457
Tiwari, A., Offringa, R., & Heuvelink, E. (2012). Auxin-induced fruit set in Capsicum annuum L. requires downstream gibberellin biosynthesis. Journal of Plant Growth Regulation, 31(4), 570-578. https://doi.org/10.1007/s00344-012-9267-7
van Huizen, R., Ozga, J. A., & Reinecke, D. M. (1997). Seed and hormonal regulation of gibberellin 20-oxidase expression in pea pericarp. Plant Physiology, 115(1), 123-128. https://doi.org/10.1104/pp.115.1.123
Vanstraelen, M., & Benková, E. (2012). Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology, 28(1), 463-487. https://doi.org/10.1146/annurev-cellbio-101011-155741
Waduthanthri K.D. (2016) Involvement of gibberellin in growth and carbohydrate partitioning in developing pea (Pisum sativum L.) seeds. MSc thesis, University of Alberta, Edmonton, AB. https://doi.org/10.7939/R3639KG6C
Wu, C., Cui, K., Wang, W., Li, Q., Fahad, S., Hu, Q., … Peng, S. (2016). Heat-induced phytohormone changes are associated with disrupted early reproductive development and reduced yield in rice. Scientific Reports, 6, 34978. https://doi.org/10.1038/srep34978
Young, L. W., Wilen, R. W., & Bonham-Smith, P. C. (2004). High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany, 55(396), 485-495. https://doi.org/10.1093/jxb/erh038
Zinn, K. E., Tunc-Ozdemir, M., & Harper, J. F. (2010). Temperature stress and plant sexual, reproduction: Uncovering the weakest links. Journal of Experimental Botany, 61(7), 1959-1968. https://doi.org/10.1093/jxb/erq053