Brassica napus (rapeseed) is the second most important oilseed crop worldwide. Global rise in average ambient temperature and extreme weather severely impact rapeseed seed yield. However, fewer research explained the phenotype changes caused by moderate-to-high temperatures in rapeseed. To investigate these events, we determined the long-term response of three spring cultivars to different temperature regimes (21/18°C, 28/18°C, and 34/18°C) mimicking natural temperature variations. The analysis focused on the plant appearance, seed yield, quality and viability, and embryo development. Our microscopic observations suggest that embryonic development is accelerated and defective in high temperatures. Reduced viable seed yield at warm ambient temperature is due to a reduced fertilization rate, increased abortion rate, defective embryonic development, and pre-harvest sprouting. Reduced auxin levels in young seeds and low ABA and auxin levels in mature seeds may cause embryo pattern defects and reduced seed dormancy, respectively. Glucosinolates and oil composition measurements suggest reduced seed quality. These identified cues help understand seed thermomorphogenesis and pave the way to developing thermoresilient rapeseed.

Hormonal Crosstalk in Plant Development Mendel Center for Plant Genomics and Proteomics CEITEC MU Central European Institute of Technology Masaryk University Brno Czechia

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Olomouc Czechia

National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czechia

Plant Sciences Core Facility Mendel Center for Plant Genomics and Proteomics CEITEC MU Central European Institute of Technology Masaryk University Brno Czechia

Research Institute of Oilseed Crops Opava Czechia

Zobrazit více v PubMed

Aksouh-Harradj N. M., Campbell L. C., Mailer R. J. (2006). Canola response to high and moderately high temperature stresses during seed maturation. Can. J. Plant Sci. 86, 967–980. doi: 10.4141/p05-130 DOI

Alexander M. P. (1969). Differential staining of aborted and nonaborted pollen. Stain. Technol. 44, 117–122. doi: 10.3109/10520296909063335, PMID: PubMed DOI

Andersen C. L., Jensen J. L., Ørntoft T. F. (2004). Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–5250. doi: 10.1158/0008-5472.can-04-0496, PMID: PubMed DOI

Angadi S. V., Cutforth H. W., Miller P. R., McConkey B. G., Entz M. H., Brandt S. A., et al. (2000). Response of three brassica species to high temperature stress during reproductive growth. Can. J. Plant Sci. 80, 693–701. doi: 10.4141/P99-152 DOI

Annisa A., Chen S., Turner N. C., Cowling W. A. (2013). Genetic variation for heat tolerance during the reproductive phase in DOI

Bac-Molenaar J. A., Fradin E. F., Becker F. F. M., Rienstra J. A., van der Schoot J., Vreugdenhil D., et al. (2015). Genome-wide association mapping of fertility reduction upon heat stress reveals developmental stage-specific QTLs in PubMed DOI PMC

Benková E., Michniewicz M., Sauer M., Teichmann T. T., Seifertová D., Juergens G., et al. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602. doi: 10.1016/s0092-8674(03)00924-3, PMID: PubMed DOI

Bieniawska Z., Espinoza C., Schlereth A., Sulpice R., Hincha D. K., Hannah M. A. (2008). Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol. 147, 263–279. doi: 10.1104/pp.108.118059, PMID: PubMed DOI PMC

Blair E. J., Bonnot T., Hummel M., Hay E., Marzolino J. M., Quijada I. A., et al. (2019). Contribution of time of day and the circadian clock to the heat stress responsive transcriptome in PubMed DOI PMC

Box M. S., Huang B. E., Domijan M., Jaeger K. E., Khattak A. K., Yoo S. J., et al. (2015). ELF3 controls thermoresponsive growth in PubMed DOI

Brooks M. E., Kristensen K., van Benthem K. J., Magnusson A., Berg C. W., Nielsen A., et al. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400. doi: 10.3929/ethz-b-000240890 DOI

Brunel-Muguet S., D’Hooghe P., Bataillé M.-P., Larré C., Kim T.-H., Trouverie J., et al. (2015). Heat stress during seed filling interferes with sulfur restriction on grain composition and seed germination in oilseed rape ( PubMed DOI PMC

Bustin S. A., Benes V., Garson J. A., Hellemans J., Huggett J., Kubista M., et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622. doi: 10.1373/clinchem.2008.112797 PubMed DOI

Castander-Olarieta A., Montalbán I. A., Oliveira E. D. M., Dell’Aversana E., D’Amelia L., Carillo P., et al. (2019). Effect of thermal stress on tissue ultrastructure and metabolite profiles during initiation of Radiata pine somatic embryogenesis. Front. Plant Sci. 9:2004. doi: 10.3389/fpls.2018.02004, PMID: PubMed DOI PMC

Celenza J. L., Quiel J. A., Smolen G. A., Merrikh H., Silvestro A. R., Normanly J., et al. (2005). The PubMed DOI PMC

Chen S., Guo Y., Sirault X., Stefanova K., Saradadevi R., Turner N. C., et al. (2019). Nondestructive phenomic tools for the prediction of heat and drought tolerance at anthesis in brassica species. Plant Phenomics 2019:3264872. doi: 10.34133/2019/3264872, PMID: PubMed DOI PMC

Chen S., Stefanova K., Siddique K. H. M., Cowling W. A. (2020a). Transient daily heat stress during the early reproductive phase disrupts pod and seed development in DOI

Chen W. W., Takahashi N., Hirata Y., Ronald J., Porco S., Davis S. J., et al. (2020b). A mobile ELF4 delivers circadian temperature information from shoots to roots. Nat. Plants 6, 416–426. doi: 10.1038/s41477-020-0634-2, PMID: PubMed DOI PMC

Chen X., Yoong F., O’Neill C. M., Penfield S. (2021). Temperature during seed maturation controls seed vigour through ABA breakdown in the endosperm and causes a passive effect on DOG1 mRNA levels during entry into quiescence. New Phytol. 232, 1311–1322. doi: 10.1111/nph.17646, PMID: PubMed DOI

Cherif A., Dubacq J., Mache R., Oursel A., Tremolieres A. (1975). Biosynthesis of α-linolenic acid by desaturation of oleic and linoleic acids in several organs of higher and lower plants and in algae. Phytochemistry 14, 703–706. doi: 10.1016/0031-9422(75)83018-4 DOI

Cruz T. M. D., Carvalho R. F., Richardson D. N., Duque P. (2014). Abscisic acid (ABA) regulation of PubMed DOI PMC

Das S., Krishnan P., Nayak M., Ramakrishnan B. (2014). High temperature stress effects on pollens of rice ( DOI

Devasirvatham V., Gaur P. M., Mallikarjuna N., Raju T. N., Trethowan R. M., Tan D. K. Y. (2013). Reproductive biology of chickpea response to heat stress in the field is associated with the performance in controlled environments. Field Crop Res. 142, 9–19. doi: 10.1016/j.fcr.2012.11.011 DOI

Doyle M. R., Davis S. J., Bastow R. M., McWatters H. G., Kozma-Bognár L., Nagy F., et al. (2002). The ELF4 gene controls circadian rhythms and flowering time in PubMed DOI

Elferjani R., Soolanayakanahally R. (2018). Canola responses to drought, heat, and combined stress: shared and specific effects on carbon assimilation, seed yield, and oil composition. Front. Plant Sci. 9:1224. doi: 10.3389/fpls.2018.01224, PMID: PubMed DOI PMC

Eom S. H., Baek S.-A., Kim J. K., Hyun T. K. (2018). Transcriptome analysis in chinese cabbage ( PubMed DOI PMC

Ezer D., Jung J.-H., Lan H., Biswas S., Gregoire L., Box M. S., et al. (2017). The evening complex coordinates environmental and endogenous signals in PubMed DOI PMC

Figueiredo D. D., Batista R. A., Roszak P. J., Hennig L., Köhler C. C. (2016). Auxin production in the endosperm drives seed coat development in PubMed DOI PMC

Figueiredo D. D., Batista R. A., Roszak P. J., Köhler C. C. (2015). Auxin production couples endosperm development to fertilization. Nat. Plants 1:15184. doi: 10.1038/nplants.2015.184, PMID: PubMed DOI

Filichkin S. A., Cumbie J. S., Dharmawardhana P., Jaiswal P., Chang J. H., Palusa S. G., et al. (2015). Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in PubMed DOI

Food and Agriculture Organization of the United Nations (2020). Available at: http://www.fao.org/faostat (Accessed January 2021).

Friml J., Vieten A., Sauer M., Weijers D., Schwarz H., Hamann T., et al. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of PubMed DOI

Gan Y., Angadi S., Cutforth H., Potts D., Angadi V., McDonald C. (2004). Canola and mustard response to short periods of temperature and water stress at different developmental stages. Can. J. Plant Sci. 84, 697–704. doi: 10.4141/P03-109 DOI

Groot S. P. C., Karssen C. M. (1992). Dormancy and germination of abscisic acid-deficient tomato seeds: studies with the PubMed DOI PMC

Guo Y., Wu W., Du M., Liu X., Wang J., Bryant C. R. (2019). Modeling climate change impacts on rice growth and yield under global warming of 1.5 and 2.0°C in the Pearl River Delta, China. Atmosphere 10:567. doi: 10.3390/atmos10100567 DOI

Hardtke C. S., Berleth T. (1998). The Arabidopsis gene PubMed DOI PMC

Hatzig S. V., Nuppenau J.-N., Snowdon R. J., Schießl S. V. (2018). Drought stress has transgenerational effects on seeds and seedlings in winter oilseed rape ( PubMed DOI PMC

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 Sci. 172, 1113–1123. doi: 10.1016/j.plantsci.2007.03.004 DOI

Hu X.-J., Chen D., Mclntyre C. L., Dreccer M. F., Zhang Z.-B., Drenth J., et al. (2018). Heat shock factor C2a serves as a proactive mechanism for heat protection in developing grains in wheat via an ABA-mediated regulatory pathway. Plant Cell Environ. 41, 79–98. doi: 10.1111/pce.12957, PMID: PubMed DOI

Hu X., Liu R., Li Y., Wang W., Tai F., Xue R., et al. (2010). Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul. 60, 225–235. doi: 10.1007/s10725-009-9436-2 DOI

Huang S., Gruber S., Stockmann F., Claupein W. (2016). Dynamics of dormancy during seed development of oilseed rape ( DOI

Huang R., Liu Z., Xing M., Yang Y., Wu X., Liu H., et al. (2019). Heat stress suppresses PubMed DOI

Impa S. M., Perumal R., Bean S. R., Sunoj V. S. J., Jagadish S. V. K. (2019). Water deficit and heat stress induced alterations in grain physico-chemical characteristics and micronutrient composition in field grown grain sorghum. J. Cereal Sci. 86, 124–131. doi: 10.1016/j.jcs.2019.01.013 DOI

ISO 659 (2009). Oilseeds - Determination of oil content (Reference method). ICS 67.200.20.

ISO 665 (2000). Oilseeds - Determination of moisture and volatile matter content. ICS : 67.200.20.

ISO 9167-1 (1992). Rapeseed - Determination of glucosinolates content - Part 1: Method using high-performance liquid chromatography. ICS : 67.200.20.

James A. B., Syed N. H., Bordage S., Marshall J., Nimmo G. A., Jenkins G. I., et al. (2012). Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24, 961–981. doi: 10.1105/tpc.111.093948, PMID: PubMed DOI PMC

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 Environ. 42, 354–372. doi: 10.1111/pce.13427, PMID: PubMed DOI

Jiang J., Liu X., Liu C., Liu G., Li S., Wang L. (2017). Integrating omics and alternative splicing reveals insights into grape response to high temperature. Plant Physiol. 173, 1502–1518. doi: 10.1104/pp.16.01305, PMID: PubMed DOI PMC

John S., Olas J. J., Roeber B. M. (2021). Regulation of alternative splicing in response to temperature variation in plants. J. Exp. Bot. 72, 6150–6163. doi: 10.1093/jxb/erab232, PMID: PubMed DOI PMC

Jumrani K., Bhatia V. S. (2014). Impact of elevated temperatures on growth and yield of chickpea ( DOI

Kanno Y., Jikumaru Y., Hanada A., Nambara E., Abrams S. R., Kamiya Y., et al. (2010). Comprehensive hormone profiling in developing PubMed DOI

Kaur H., Ozga J. A., Reinecke D. M. (2020). Balancing of hormonal biosynthesis and catabolism pathways, a strategy to ameliorate the negative effects of heat stress on reproductive growth. Plant Cell Environ. 44, 1486–1503. doi: 10.1111/pce.13820, PMID: PubMed DOI

Koscielny C. B., Hazebroek J., Duncan R. W. (2018). Phenotypic and metabolic variation among spring DOI

Kulichová K., Kumar V., Steinbachová L., Klodová B., Timofejeva L., Juříček M., et al. (2020). PRP8A and PRP8B spliceosome subunits act coordinately to control pollen tube attraction in PubMed DOI

Kumar S. V., Lucyshyn D., Jaeger K. E., Alós E., Alvey E., Harberd N. P., et al. (2012). PHYTOCHROME INTERACTING FACTOR4 controls the thermosensory activation of flowering. Nature 484, 242–245. doi: 10.1038/nature10928, PMID: PubMed DOI PMC

Lefebvre V., North H., Frey A., Sotta B., Seo M. M., Okamoto M., et al. (2006). Functional analysis of PubMed DOI

Lesk C., Rowhani P., Ramankutty N. (2016). Influence of extreme weather disasters on global crop production. Nature 529, 84–87. doi: 10.1038/nature16467, PMID: PubMed DOI

Li M., Cao L., Mwimba M., Zhou Y., Li L., Zhou M., et al. (2019). Comprehensive mapping of abiotic stress inputs into the soybean circadian clock. Proc. Natl. Acad. Sci. U.S.A. 116, 23840–23849. doi: 10.1073/pnas.1708508116, PMID: PubMed DOI PMC

Li H., Liu S.-S., Yi C.-Y., Wang F., Zhou J., Xia X.-J., et al. (2014). Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant Cell Environ. 37, 2768–2780. doi: 10.1111/pce.12360, PMID: PubMed DOI

Lin C.-J., Li C.-Y., Lin S.-K., Yang F.-H., Huang J.-J., Liu Y.-H., et al. (2010). Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in rice ( PubMed DOI

Lin K., Zhao H., Gan S., Li G. (2019). Arabidopsis ELF4-like proteins EFL1 and EFL3 influence flowering time. Gene 700, 131–138. doi: 10.1016/j.gene.2019.03.047, PMID: PubMed DOI

Liu B., Asseng S., Müller C., Ewert F., Elliott J., Lobell D. B., et al. (2016). Similar estimates of temperature impacts on global wheat yield by three independent methods. Nat. Clim. Chang. 6, 1130–1136. doi: 10.1038/nclimate3115 DOI

Liu L., Liu F., Chu J., Yi X., Fan W., Tang T., et al. (2019). A transcriptome analysis reveals a role for the indole GLS-linked auxin biosynthesis in secondary dormancy in rapeseed ( PubMed DOI PMC

Liu X., Wang X., Wang X., Gao J., Luo N., Meng Q., et al. (2020). Dissecting the critical stage in the response of maize kernel set to individual and combined drought and heat stress around flowering. Environ. Exp. Bot. 179:104213. doi: 10.1016/j.envexpbot.2020.104213 DOI

Liu X., Zhang H., Zhao Y., Feng Z., Li Q., Yang H.-Q., et al. (2013). Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in PubMed DOI PMC

Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2 PubMed DOI

Lu W., Tang X., Huo Y., Xu R., Qi S., Huang J., et al. (2012). Identification and characterization of fructose 1,6-bisphosphate aldolase genes in PubMed DOI

Ludwig-Müller J., Krishna P., Forreiter C. (2000). A glucosinolate mutant of PubMed DOI PMC

Luo Q. (2011). Temperature thresholds and crop production: a review. Clim. Chang. 109, 583–598. doi: 10.1007/s10584-011-0028-6 DOI

Marutani M., Sheffer R. D., Kamemoto H. (1993). Cytological analysis of DOI

McCulloch C. E., Neuhaus J. M. (2005). “Generalized linear mixed models,” in Encyclopedia of Biostatistics. eds. Armitage P., Colton T. (Chischester, UK: Wiley; ).

McWatters H. G., Kolmos E., Hall A., Doyle M. R., Amasino R. M., Gyula P., et al. (2007). ELF4 is required for oscillatory properties of the circadian clock. Plant Physiol. 144, 391–401. doi: 10.1104/pp.107.096206, PMID: PubMed DOI PMC

Mellor N., Band L. R., Pencík A., Novak O., Rashed A., Holman T., et al. (2016). Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proc. Natl. Acad. Sci. U.S.A. 113, 11022–11027. doi: 10.1073/pnas.1604458113, PMID: PubMed DOI PMC

Morrison M. J., McVetty P. B. E., Shaykewich C. F. (1989). The determination and verification of a baseline temperature for the growth of Westar summer rape. Can. J. Plant Sci. 69, 455–464. doi: 10.4141/cjps89-057 DOI

Morrison M. J., Stewart D. W. (2002). Heat stress during flowering in summer brassica. Crop Sci. 42, 797–803. doi: 10.2135/cropsci2002.7970 DOI

Pěnčík A., Casanova-Sáez R., Pilařová V., Žukauskaitė A., Pinto R., Micol J. L., et al. (2018). Ultra-rapid auxin metabolite profiling for high-throughput mutant screening in Arabidopsis. J. Exp. Bot. 69, 2569–2579. doi: 10.1093/jxb/ery084, PMID: PubMed DOI PMC

Peng S., Huang J., Sheehy J. E., Laza R. C., Visperas R. M., Zhong X., et al. (2004). Rice yields decline with higher night temperature from global warming. Proc. Natl. Acad. Sci. U.S.A. 101, 9971–9975. doi: 10.1073/pnas.0403720101, PMID: PubMed DOI PMC

Pérez-Alonso M.-M., Ortiz-García P., Moya-Cuevas J., Lehmann T., Sánchez-Parra B., Björk R. G., et al. (2021). Endogenous indole-3-acetamide levels contribute to the crosstalk between auxin and abscisic acid, and trigger plant stress responses in PubMed DOI PMC

Pfaffl M. W., Tichopad A., Prgomet C., Neuvians T. P. (2004). Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol. Lett. 26, 509–515. doi: 10.1023/b:bile.0000019559.84305.47 PubMed DOI

Polowick P. L., Sawhney V. K. (1988). High-temperature induced male and female sterility in canola ( DOI

Prigge M. J., Platre M., Kadakia N., Zhang Y., Greenham K., Szutu W., et al. (2020). Genetic analysis of the PubMed DOI PMC

Rademacher E. H., Lokerse A. S., Schlereth A., Peris C. L., Bayer M., Kientz M., et al. (2012). Different auxin response machineries control distinct cell fates in the early plant embryo. Dev. Cell 22, 211–222. doi: 10.1016/j.devcel.2011.10.026, PMID: PubMed DOI

Radoeva T., Lokerse A. S., Peris C. L., Wendrich J. R., Xiang D., Liao C.-Y., et al. (2019). A robust auxin response network controls embryo and suspensor development through a basic helix loop helix transcriptional module. Plant Cell 31, 52–67. doi: 10.1105/tpc.18.00518, PMID: PubMed DOI PMC

Rae G. M., Uversky V. N., David K. M., Wood M. (2014). DRM1 and DRM2 expression regulation: potential role of splice variants in response to stress and environmental factors in PubMed DOI

Rao S.-Q., Chen X.-Q., Wang K.-H., Zhu Z.-J., Yang J., Zhu B. (2021). Effect of short-term high temperature on the accumulation of glucosinolates in PubMed DOI

R Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/ (Accessed November 20, 2020).

Robert H. S., Grones P., Stepanova A. N., Robles L. M., Lokerse A. S., Alonso J. M., et al. (2013). Local auxin sources orient the apical-basal axis in PubMed DOI

Robert H. S., Grunewald W., Sauer M., Cannoot B., Soriano M., Swarup R., et al. (2015). Plant embryogenesis requires AUX/LAX-mediated auxin influx. Development 142, 702–711. doi: 10.1242/dev.115832, PMID: PubMed DOI

Robert H. S., Park C., Gutièrrez C. L., Wójcikowska B., Pencík A., Novak O., et al. (2018). Maternal auxin supply contributes to early embryo patterning in PubMed DOI PMC

RStudio Team (2019). RStudio: Integrated Development for R. RStudio, PBC, Inc. Boston, MA, USA. Available at: http://www.rstudio.com/ (Accessed November 20, 2020).

Russell (2020). Emmeans: Estimated Marginal Means, Aka Least-Squares Means, R Package Version 1.4.5; 2020. Available at: https://cran.r-project.org/web/packages/emmeans/index.html (Accessed December 20, 2020).

Salehin M., Li B., Tang M., Katz E., Song L., Ecker J. R., et al. (2019). Auxin-sensitive aux/IAA proteins mediate drought tolerance in PubMed DOI PMC

Sanchez A., Shin J., Davis S. J. (2011). Abiotic stress and the plant circadian clock. Plant Signal. Behav. 6, 223–231. doi: 10.4161/psb.6.2.14893, PMID: PubMed DOI PMC

Sánchez-Parra B., Pérez-Alonso M.-M., Ortiz-García P., Moya-Cuevas J., Hentrich M., Pollmann S. (2021). Accumulation of the auxin precursor indole-3-acetamide curtails growth through the repression of ribosome-biogenesis and development-related transcriptional networks. Int. J. Mol. Sci. 22:2040. doi: 10.3390/ijms22042040, PMID: PubMed DOI PMC

Seaton D. D., Toledo-Ortiz G., Ganpudi A., Kubota A., Imaizumi T., Halliday K. J. (2018). Dawn and photoperiod sensing by phytochrome A. Proc. Natl. Acad. Sci. U.S.A. 115, 10523–10528. doi: 10.1073/pnas.1803398115, PMID: PubMed DOI PMC

Seo M. M., Hanada A., Kuwahara A., Endo A., Okamoto M., Yamauchi Y., et al. (2006). Regulation of hormone metabolism in PubMed DOI

Singh R. P., Prasad P. V. V., Sunita K., Giri S. N., Reddy K. R. (2007). Influence of high temperature and breeding for heat tolerance in cotton: a review. Adv. Agron. 93, 313–385. doi: 10.1016/S0065-2113(06)93006-5 DOI

Singh A. K., Singh M. K., Singh V., Singh R., Raghuvanshi T., Singh C. (2017). Debilitation in tomato (

Slane D., Lee C. H., Kolb M., Dent C., Miao Y., Franz-Wachtel M., et al. (2020). The integral spliceosomal component CWC15 is required for development in PubMed DOI PMC

Song Y. H., Kubota A., Kwon M. S., Covington M. F., Lee N., Taagen E. R., et al. (2018). Molecular basis of flowering under natural long-day conditions in PubMed DOI PMC

Stavang J. A., Gallego-Bartolomé J., Gómez M. D., Yoshida S., Asami T., Olsen J. E., et al. (2009). Hormonal regulation of temperature-induced growth in PubMed DOI

Sugliani M., Brambilla V., Clerkx E. J. M., Koornneef M., Soppe W. J. J. (2010). The conserved splicing factor SUA controls alternative splicing of the developmental regulator ABI3 in PubMed DOI PMC

Talukder A. S. M. H. M., McDonald G. K., Gill G. S. (2014). Effect of short-term heat stress prior to flowering and early grain set on the grain yield of wheat. Field Crop Res. 160, 54–63. doi: 10.1016/j.fcr.2014.01.013 DOI

Torres C. A., Sepúlveda G., Kahlaoui B. (2017). Phytohormone interaction modulating fruit responses to photooxidative and heat stress on apple ( PubMed DOI PMC

Tuteja N. (2007). Abscisic acid and abiotic stress signaling. Plant Signal. Behav. 2, 135–138. doi: 10.4161/psb.2.3.4156, PMID: PubMed DOI PMC

Vandesompele J., Preter K. D., Pattyn F., Poppe B., Roy N. V., Paepe A. D., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034. doi: 10.1186/gb-2002-3-7-research0034, PMID: PubMed DOI PMC

Verma S., Attuluri V. P. S., Robert H. S. (2021). An essential function for auxin in embryo development. CSH Perspect. Biol. 13:a039966. doi: 10.1101/cshperspect.a039966, PMID: PubMed DOI PMC

Vishwakarma K., Upadhyay N., Kumar N., Yadav G., Singh J., Mishra R. K., et al. (2017). Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 8:161. doi: 10.3389/fpls.2017.00161, PMID: PubMed DOI PMC

Vu L. D., Xu X., Gevaert K., Smet I. D. (2019). Developmental plasticity at high temperature. Plant Physiol. 181, 399–411. doi: 10.1104/pp.19.00652, PMID: PubMed DOI PMC

Wojtaczka P., Ciarkowska A., Starzynska E., Ostrowski M. (2022). The GH3 amidosynthetases family and their role in metabolic crosstalk modulation of plant signaling compounds. Phytochemistry 194:113039. doi: 10.1016/j.phytochem.2021.113039, PMID: PubMed DOI

Wu C., Cui K., Wang W., Li Q., Fahad S., Hu Q., et al. (2016). Heat-induced phytohormone changes are associated with disrupted early reproductive development and reduced yield in rice. Sci. Rep. 6, 34978–34914. doi: 10.1038/srep34978, PMID: PubMed DOI PMC

Young L. W., Wilen R. W., Bonham-Smith P. C. (2004). High temperature stress of PubMed DOI

Zhang H., Liu Y., Wen F., Yao D., Wang L., Guo J., et al. (2014). A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. J. Exp. Bot. 65, 5795–5809. doi: 10.1093/jxb/eru313, PMID: PubMed DOI PMC

Zhao C., Liu B., Piao S., Wang X., Lobell D. B., Huang Y., et al. (2017). Temperature increase reduces global yields of major crops in four independent estimates. Proc. Natl. Acad. Sci. U.S.A. 114, 9326–9331. doi: 10.1073/pnas.1701762114, PMID: PubMed DOI PMC

Integrative phenotyping analyses reveal the relevance of the phyB-PIF4 pathway in Arabidopsis thaliana reproductive organs at high ambient temperature

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus