Identification of transcriptional modules linked to the drought response of Brassica napus during seed development and their mitigation by early biotic stress.

Publisher: Scandinavian Society For Plant Physiology Country of Publication: Denmark NLM ID: 1256322 Publication Model: Print Cited Medium: Internet ISSN: 1399-3054 (Electronic) Linking ISSN: 00319317 NLM ISO Abbreviation: Physiol Plant Subsets: MEDLINE

Publication: Copenhagen : Scandinavian Society For Plant Physiology
Original Publication: Lund, Sweden [etc.]

Brassica napus*/genetics ; Brassica napus*/physiology ; Seeds*/genetics ; Seeds*/growth & development ; Droughts* ; Gene Expression Regulation, Plant* ; Stress, Physiological*/genetics; Plant Proteins/genetics ; Plant Proteins/metabolism ; Plasmodiophorida/physiology ; Transcriptome/genetics

In order to capture the drought impacts on seed quality acquisition in Brassica napus and its potential interaction with early biotic stress, seeds of the 'Express' genotype of oilseed rape were characterized from late embryogenesis to full maturity from plants submitted to reduced watering (WS) with or without pre-occurring inoculation by the telluric pathogen Plasmodiophora brassicae (Pb + WS or Pb, respectively), and compared to control conditions (C). Drought as a single constraint led to significantly lower accumulation of lipids, higher protein content and reduced longevity of the WS-treated seeds. In contrast, when water shortage was preceded by clubroot infection, these phenotypic differences were completely abolished despite the upregulation of the drought sensor RD20. A weighted gene co-expression network of seed development in oilseed rape was generated using 72 transcriptomes from developing seeds from the four treatments and identified 33 modules. Module 29 was highly enriched in heat shock proteins and chaperones that showed a stronger upregulation in Pb + WS compared to the WS condition, pointing to a possible priming effect by the early P. brassicae infection on seed quality acquisition. Module 13 was enriched with genes encoding 12S and 2S seed storage proteins, with the latter being strongly upregulated under WS conditions. Cis-element promotor enrichment identified PEI1/TZF6, FUS3 and bZIP68 as putative regulators significantly upregulated upon WS compared to Pb + WS. Our results provide a temporal co-expression atlas of seed development in oilseed rape and will serve as a resource to characterize the plant response towards combinations of biotic and abiotic stresses.
(© 2024 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.)

Aguilar, E., Cutrona, C., Del Toro, F.J., Vallarino, J.G., Osorio, S., Pérez‐Bueno, M.L., Barón, M., Chung, B.‐N., Canto, T. and Tenllado, F. (2017) Virulence determines beneficial trade‐offs in the response of virus‐infected plants to drought via induction of salicylic acid. Plant Cell Environ., 40, 2909–2930. https://doi.org/10.1111/pce.13028.
Aigu, Y., Laperche, A., Mendes, J., Lariagon, C., Guichard, S., Gravot, A. and Manzanares‐Dauleux, M.J. (2018) Nitrogen supply exerts a major/minor switch between two QTLs controlling Plasmodiophora brassicae spore content in rapeseed. Plant Pathol., 67, 1574–1581. https://doi.org/10.1111/ppa.12867.
Aigu, Y., Cao, T., Strelkov, I.S., Manolii, V.P., Lemoine, J., Manzanares‐Dauleux, M.J., Strelkov, S.E. and Gravot, A. (2020) Identification of winter and spring Brassica napus genotypes with partial resistance to Canadian isolates of Plasmodiophora brassicae. Can. J. Plant Pathol., 42, 538–546. https://doi.org/10.1080/07060661.2020.1723870.
Aigu, Y., Daval, S., Gazengel, K., Marnet, N., Lariagon, C., Laperche, A., Legeai, F., Manzanares‐Dauleux, M.J. and Gravot, A. (2022) Multi‐omic investigation of low‐nitrogen conditional resistance to clubroot reveals Brassica napus genes involved in nitrate assimilation. Front. Plant Sci., 11. https://doi.org/10.3389/fpls.2022.790563.
Alexa, A., Rahnenführer, J. and Lengauer, T. (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics, 22, 1600–1607. https://doi.org/10.1093/bioinformatics/btl140.
Alexander, R.D., Castillejo‐Pons, P., Alsaif, O., Stahl, Y., Seale, M. and Morris, P.C. (2020) The conserved plant PM19 protein functions as an osmosensor and regulator of germination. bioRxiv, https://doi.org/10.1101/2020.08.10.244889.
Atkinson, N.J. and Urwin, P.E. (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot., 63, 3523–3543. https://doi.org/10.1093/jxb/ers100.
Baldini, M., Giovanardi, R., Tahmasebi Enferadi, S. and Vannozzi, G. (2002) Effects of water regime on fatty acid accumulation and final fatty acid composition in the oil of standard and high oleic sunflower hybrids. Ital. J. Agron., 6, 119–126.
Barcala, M., García, A., Cubas, P., Almoguera, C., Jordano, J., Fenoll, C. and Escobar, C. (2008) Distinct heat‐shock element arrangements that mediate the heat shock, but not the late‐embryogenesis induction of small heat‐shock proteins, correlate with promoter activation in root‐knot nematode feeding cells. Plant Mol. Biol., 66, 151–164. https://doi.org/10.1007/s11103-007-9259-3.
Barnabas, B., Jager, K. and Feher, A. (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Env., 31, 11–38. https://doi.org/10.1111/j.1365-3040.2007.01727.x.
Barthet, V.J. and Daun, J.K. (2011) Seed morphology, composition, and quality. In Canola: chemistry, production, processing, and utilization (Daun, J.K., Michael Eskin, N.A. and Hickling D., eds). Canola, AOCS Press, pp. 119–162. https://doi.org/10.1016/B978-0-9818936-5-5.50009-7.
Basbouss‐Serhal, I., Soubigou‐Taconnat, L., Bailly, C. and Leymarie, J. (2015) Germination potential of dormant and nondormant Arabidopsis seeds is driven by distinct recruitment of messenger RNAs to polysomes. Plant Physiol., 168, 1049–1065. https://doi.org/10.1104/pp.15.00510.
Baud, S., Boutin, J‐P., Miquel, M., Lepiniec, L. and Rochat, C. (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem., 40, 151–160. https://doi.org/10.1016/S0981-9428(01)01350-X.
Baud, S., Dubreucq, B., Miquel, M., Rochat, C. and Lepiniec, L. (2008) Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. In The arabidopsis book, 6, e0113. https://doi.org/10.1199/tab.0113.
Becker, M.G., Walker, P.L., Pulgar‐Vidal, N.C. and Belmonte, M.F. (2017) SeqEnrich: A tool to predict transcription factor networks from co‐expressed Arabidopsis and Brassica napus gene sets. PLoS One, 12, e0178256. https://doi.org/10.1371/journal.pone.0178256.
Bensmihen, S., Rippa, S., Lambert, G., Jublot, D., Pautot, V., Granier, F., Giraudat, J. and Parcy, F. (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine‐tune gene expression during late embryogenesis. Plant Cell, 14, 1391–1403. https://doi.org/10.1105/tpc.000869.
Bewley, J.D., Bradford, K.J., Hilhorst, H.W.M. and Nonogaki, H. (2013) Seeds: Physiology of development, germination and dormancy. 3rd Edition, Springer, New York. https://doi.org/10.1007/978-1-4614-4693-4.
Bianchetti, G., Clouet, V., Legeai, F., Gazengel, K., Baron, C., Carrillo, A., Manzanares‐Dauleux, M.J., Buitink, J. and Nesi, N. (2021a) RNA sequencing data for responses to drought stress and/or clubroot infection in developing seeds of Brassica napus. Data Br., 38, 107392. https://doi.org/10.1016/j.dib.2021.107392.
Bianchetti, G., Baron, C., Carrillo, A., Berardocco, S., Marnet, N., Wagner, M‐H., Demilly, D., Ducournau, S., Manzanares‐Dauleux, M.J., Le Cahérec, F., Buitink, J. and Nesi, N. (2021b) Dataset for the metabolic and physiological characterization of seeds from oilseed rape (Brassica napus L.) plants grown under single or combined effects of drought and clubroot pathogen Plasmodiophora brassicae. Data Br., 37, 107247. https://doi.org/10.1016/j.dib.2021.107247.
Bizouerne, E., Buitink, J., Ly Vu, B., Ly Vu, J., Esteban, E., Pasha, A., Provart, N., Verdier, J. and Leprince, O. (2021) Gene co‐expression analysis of tomato seed maturation reveals tissue‐specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour. BMC Plant Biol., 21, 124. https://doi.org/10.1186/s12870-021-02889-8.
Bogamuwa, S. and Jang, J.C. (2016) Plant tandem CCCH zinc finger proteins interact with ABA, drought, and stress response regulators in processing‐bodies and stress granules. PLoS One, 11, e0151574. https://doi.org/10.1371/journal.pone.0151574.
Borisjuk, L., Neuberger, T., Schwender, J., Heinzel, N., Sunderhaus, S., Fuchs, J., Hay, J.O., Tschiersch, H., Braun, H.‐P., Denolf, P., et al. (2013) Seed architecture shapes embryo metabolism in oilseed rape. Plant Cell, 25, 1625–1640. https://doi.org/10.1105/tpc.113.111740.
Bouchereau, A., Clossais‐Besnard, N., Bensaoud, A., Leport, L. and Renard, M. (1996) Water stress effects on rapeseed quality. Eur. J. Agron., 5, 19–30. https://doi.org/10.1016/S1161-0301(96)02005-9.
Brunel‐Muguet, S., D'Hooghe, P., Bataillé, M‐P., Larré, C., Kim, T‐H., Trouverie, J., Avice, J‐C., Etienne, P. and Dürr, C. (2015) Heat stress during seed filling interferes with sulfur restriction on grain composition and seed germination in oilseed rape (Brassica napus L.). Front. Plant Sci., 6, 213. https://doi.org/10.3389/fpls.2015.01236.
Chalhoub, B., Denoeud, F., Liu, S., Parkin, I.A.P., Tang, H., et al. (2014) Early allopolyploid evolution in the post‐Neolithic Brassica napus oilseed genome. Science, 345, 950–953. https://doi.org/10.1126/science.1253435.
Champolivier, L. and Merrien, A. (1996) Effects of water stress applied at different growth stages to Brassica napus L. var. oleifera on yield, yield components and seed quality. Eur. J. Agron., 5, 153–160. https://doi.org/10.1016/S1161-0301(96)02004-7.
Chern, M.S., Eiben, H.G. and Bustos, M.M. (1996) The developmentally regulated bZIP factor ROM1 modulates transcription from lectin and storage protein genes in bean embryos. Plant J., 10, 135–148. https://doi.org/10.1046/j.1365-313X.1996.10010135.x.
Chia, T.Y.P., Pike, M.J. and Rawsthorne, S. (2005) Storage oil breakdown during embryo development of Brassica napus (L.). J. Exp. Bot., 56, 1285–1296. https://doi.org/10.1093/jxb/eri129.
Ciaghi, S., Schwelm, A. and Neuhauser, S. (2019) Transcriptomic response in symptomless roots of clubroot infected kohlrabi (Brassica oleracea var. gongylodes) mirrors resistant plants. BMC Plant Biol., 19, 288. https://doi.org/10.1186/s12870-019-1902-z.
Creus, C.M., Sueldo, R.J. and Barassi, C.A. (2004) Water relations and yield in Azospirillum‐inoculated wheat exposed to drought in the field. Can. J. Bot., 82, 273–281. https://doi.org/10.1139/b03-119.
Ding, Y., Fromm, M. and Avramova, Z. (2012) Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat. Commun., 3, 740. https://doi.org/10.1038/ncomms1732.
Dixon, G.R. (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J. Plant Growth Regul., 28, 194–202. https://doi.org/10.1007/s00344-009-9090-y.
Elferjani, R. and 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. https://doi.org/10.3389/fpls.2018.01224.
Ewels, P.A., Peltzer, A., Fillinger, S., Patel, H., Alneberg, J., Wilm, A., Garcia, M.U., Di Tommaso, P. and Nahnsen, S. (2020) The nf‐core framework for community‐curated bioinformatics pipelines. Nat. Biotechnol., 38, 276–278. https://doi.org/10.1038/s41587-020-0439-x.
Farooq, M., Hussain, M. and Siddique, K.H.M. (2014) Drought stress in wheat during flowering and grain‐filling periods. Critic. Rev. Plant Sci., 33, 331–349. https://doi.org/10.1080/07352689.2014.875291.
Fatihi, A., Boulard, C., Bouyer, D. Baud, S., Dubreucq, B. and Lepiniec, L. (2016) Deciphering and modifying LAFL transcriptional regulatory network in seed for improving yield and quality of storage compounds. Plant Sci., 250, 198–204. https://doi.org/10.1016/j.plantsci.2016.06.013.
Ghazalpour, A., Doss, S., Zhang, B., Wang, S., Plaisier, C., Castellanos, R., et al. (2006) Integrating genetic and network analysis to characterize genes related to mouse weight. PLoS Genet., 2, 1182–1192. https://doi.org/10.1371/journal.pgen.0020130.
Goldberg, R.B., de Paiva, G. and Yadegari, R. (1994) Plant embryogenesis: Zygote to seed. Science, 266, 605–614. DOI: https://doi.org/10.1126/science.266.5185.605.
Gravot, A., Lemarié, S., Richard, G., Lime, T., Lariagon, C. and Manzanares‐Dauleux, M.J. (2016) Flooding affects the post‐invasive development of Plasmodiophora brassicae in Arabidopsis roots during the secondary phase of infection. Plant Pathol., 65, 1153–1160. https://doi.org/10.1111/ppa.12487.
Hatzig, S.V., Nuppenau, J‐N., Snowdon, R.J. and Schießl, S.V. (2018) Drought stress has transgenerational effects on seeds and seedlings in winter oilseed rape (Brassica napus L.). BMC Plant Biol., 18, 297. https://doi.org/10.1186/s12870-018-1531-y.
Havé, M., Marmagne, A., Chardon, F. and Masclaux‐Daubresse, C. (2017) Nitrogen remobilization during leaf senescence: lessons from Arabidopsis to crops. J. Exp. Bot., 68, 2513–2529. https://doi.org/10.1093/jxb/erw365.
Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt, S., et al. (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev. Camb. Phil. Soc., 91, 1118–1133. https://doi.org/10.1111/brv.12215.
Kim, D., Paggi, J.M., Park, C., Bennett, C. and Salzberg S.L. (2019) Graph‐based genome alignment and genotyping with HISAT2 and HISAT‐genotype Graph‐based genome alignment and genotyping with HISAT2 and HISAT‐genotype. Nat. Biotechnol., 37, 907–915. https://doi.org/10.1038/s41587-019-0201-4.
Kotak, S., Vierling, E., Bäumlein, H. and von Koskull‐Döring, P. (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell, 19, 182–195. https://doi.org/10.1105/tpc.106.048165.
Lancashire, P.D., Bleiholder, H., Boom, T.V.D., Langelüddeke, P., Stauss, R., Weber, E. and Witzenberger, A. (1991) A uniform decimal code for growth stages of crops and weeds. Ann. Appl. Biol., 119, 561–601. https://doi.org/10.1111/j.1744-7348.1991.tb04895.x.
Langfelder, P. and Horvath, S. (2008) WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559. https://doi.org/10.1186/1471-2105-9-559.
Laperche, A., Aigu, Y., Jubault, M., Ollier, M., Guichard, S., Glory, P., Strelkov, S.E., Gravot, A. and Manzanares‐Dauleux, M.J. (2017) Clubroot resistance QTL are modulated by nitrogen input in Brassica napus. Theor. Appl. Genet., 130, 669–684. https://doi.org/10.1007/s00122-016-2842-8.
Le, B.H., Cheng, C., Bui, A.Q., Wagmaister, J.A., Henry, K.F., Pelletier, J., Kwong, L., Belmonte, M., Kirkbride, R., Horvath, S., Drews, G.N., Fischer, R.L., Okamuro, J.K., Harada, J.J. and Goldberg, R.B. (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed‐specific transcription factors. Proc. Natl. Acad. Sci. USA, 107, 8063–8070. https://doi.org/10.1073/pnas.1003530107.
Leprince, O., Pellizzaro, A., Berrir, S. and Buitink, J. (2017) Late seed maturation: drying without dying. J. Exp. Bot., 68, 827–841. https://doi.org/10.1093/jxb/erw363.
Lê, S., Josse, J., and Husson, F. (2008). FactoMineR: an R package for multivariate analysis. Journal of statistical software, 25, 1‐18.Li, Z. and Thomas, T.L. (1998) PEI1, an embryo‐specific zinc finger protein gene required for heart‐stage embryo formation in Arabidopsis. Plant Cell, 10, 383–398. https://doi.org/10.1105/tpc.10.3.383.
Li, Y., Beisson, F., Pollard, M. and Ohlrogge, J. (2006) Oil content of Arabidopsis seeds: the influence of seed anatomy, light and plant‐to‐plant variation. Phytochemistry, 67, 904–915. https://doi.org/10.1016/j.phytochem.2006.02.015.
Li, Y., Ye, W., Wang, M. and Yan, X. (2009) Climate change and drought. A risk assessment of crop‐yield impacts. Clim. Res., 39, 31–46. https://doi.org/10.3354/cr00797.
Li, Y., Liu, W., Zhong, H., Zhang, H.‐L. and Xia, Y. (2019) Redox‐sensitive bZIP68 plays a role in balancing stress tolerance with growth in Arabidopsis. Plant J., 100, 768–783. https://doi.org/10.1111/tpj.14476.
Liao, Y., Smyth, G.K. and Shi, W. (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923–930. https://doi.org/10.1093/bioinformatics/btt656.
Liégard, B., Baillet, V., Etcheverry, M., Joseph, E., Lariagon, C., Lemoine, J., Evrard, A., Colot, V., Gravot, A., Manzanares‐Dauleux, M.J. and Jubault, M. (2019) Quantitative resistance to clubroot infection mediated by transgenerational epigenetic variation in Arabidopsis. New Phytol., 222, 468–479. https://doi.org/10.1111/nph.15579.
Liu, Y.‐H., Offler, C.E. and Ruan, Y.‐L. (2013) Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals. Front. Plant Sci., 4, 282. https://doi.org/10.3389/fpls.2013.00282.
Locascio, A., Roig‐Villanova, I., Bernardi, J. and Varotto, S. (2014) Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Front. Plant Sci., 5, 412. https://doi.org/10.3389/fpls.2014.00412.
Ludwig‐Müller, J., Prinsen, E., Rolfe, S.A. and Scholes, J.D. (2009) Metabolism and plant hormone action during clubroot disease. J. Plant Growth Regul., 28, 229–244. https://doi.org/10.1007/s00344-009-9089-4.
Mittler, R. (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci., 11, 15–19. https://doi.org/10.1016/j.tplants.2005.11.002.
Manzanares‐Dauleux, M.J., Divaret, I., Baron, F. and Thomas G. (2000a) Evaluation of French Brassica oleracea landraces for resistance to Plasmodiophora brassicae. Euphytica, 113, 211–218. https://doi.org/10.1023/A:1003997421340.
Manzanares‐Dauleux, M.J., Delourme, R., Baron, F. and Thomas, G. (2000b) Mapping of one major gene and of QTLs involved in resistance to clubroot in Brassica napus. Theor. Appl. Genet., 101, 885–891. https://doi.org/10.1007/s001220051557.
Meinke, D.W., Franzmann, L.H., Nickle, T.C. and Yeung, E.C. (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell, 6, 1049–1064. https://doi.org/10.1105/tpc.6.8.1049.
Nambara, E., Naito, S. and McCourt, P. (1992) A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. Plant J., 2, 435–441. https://doi.org/10.1111/j.1365-313X.1992.00435.x.
Nesi, N., Delourme, R., Brégeon, M., Falentin, C. and Renard, M. (2008) Genetic and molecular approaches to improve nutritional value of Brassica napus L. seed. C. R. Biol., 331, 763–771. https://doi.org/10.1016/j.crvi.2008.07.018.
Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K. and Shigeoka, S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J., 48, 535–547. https://doi.org/10.1111/j.1365-313X.2006.02889.x.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2015) Vegan: community ecology package. R package vegan, vers. 2.5‐7. Retrieved on September 21th, 2021, from http://CRAN.Rproject.org/package=vegan2015.
Pageau, D., Lajeunesse, J. and Lafond, J. (2006) Impact of clubroot (Plasmodiophora brassicae) on the yield and quality of canola. Can. J. Plant Pathol., 28, 137–143.
Pandey, P., Irulappan, V., Bagavathiannan, M.V. and Senthil‐Kumar, M. (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio‐morphological traits. Front. Plant Sci., 8, 537. https://doi.org/10.3389/fpls.2017.00537.
Park, C.J. and Seo, Y.S. (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol. J., 31, 323–333. https://doi.org/10.5423/PPJ.RW.08.2015.0150.
Rae, G.M., Uversky, V.N., David, K. and Wood, M. (2014) DRM1 and DRM2 expression regulation: potential role of splice variants in response to stress and environmental factors in Arabidopsis. Mol. Gen. Genomics, 289, 317–332. https://doi.org/10.1007/s00438-013-0804-2.
Rajjou, L. and Debeaujon, I. (2008) Seed longevity: Survival and maintenance of high germination ability of dry seeds. C. R. Biol., 331, 796–805. https://doi.org/10.1016/j.crvi.2008.07.021.
Ramegowda, V. and Senthil‐Kumar, M. (2015) The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J. Plant Physiol., 176, 47–54. https://doi.org/10.1016/j.jplph.2014.11.008.
Rasmussen, S., Barah, P., Suarez‐Rodriguez, M.C., Bressendorff, S., Friis, P., Costantino, P., Bones, A.M., Nielsen, H.B. and Mundy, J. (2013) Transcriptome responses to combinations of stresses in Arabidopsis, Plant Physiol., 161, 1783–1794. https://doi.org/10.1104/pp.112.210773.
Righetti, K., Vu, J.L., Pelletier, S., Vu, B.L., Glaab, E., Lalanne, D., Pasha, A., Patel, R.V., Provart, N.J., Verdier, J., et al. (2015) Inference of longevity‐related genes from a robust coexpression network of seed maturation identifies regulators linking seed storability to biotic defense‐related pathways. Plant Cell, 27, 2692–2708. https://doi.org/10.1105/tpc.15.00632.
Rousseau‐Gueutin, M., Belser, C., Da Silva, C., Richard, G., Istace, B., Cruaud, C., Falentin, C. et al. (2020) Long‐read assembly of the Brassica napus reference genome Darmor‐bzh. GigaScience, 9, giaa137.
Roy, S., Saxena, S., Sinha, A. and Nandi, A.K. (2020) DORMANCY/AUXIN ASSOCIATED FAMILY PROTEIN 2 of Arabidopsis thaliana is a negative regulator of local and systemic acquired resistance. J. Plant Res., 133, 409–417. https://doi.org/10.1007/s10265-020-01183-2.
Santos‐Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Caboche, M. and Lepiniec, L. (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J., 54, 608–620. https://doi.org/10.1111/j.1365-313X.2008.03461.x.
Sehgal, A., Sita, K., Siddique, K.H.M., Kumar, R., Bhogireddy, S., Varshney, R.K., HanumanthaRao, B., Nair, R.M., Prasad, P.V.V. and Nayyar, H. (2018) Drought or/and heat‐stress effects on seed filling in food crops: impacts on functional biochemistry, seed yields, and nutritional quality. Front. Plant Sci., 9, 1705. https://doi.org/10.3389/fpls.2018.01705.
Stagnari, F., Galieni, A. and Pisante, M. (2016) Drought stress effects on crop quality. In Water Stress and Crop Plants: A Sustainable Approach (Ahmad, P., eds). Chichester, UK: Wiley, pp. 375–392.
Strehlow, B., de Mol, F. and Struck, C. (2015) Risk potential of Clubroot disease on winter oilseed rape. Plant Dis., 99, 667–675. https://doi.org/10.1094/PDIS-05-14-0482-RE.
Strelkov, S.E., Hwang, S.F., Manolii, V.P., Turnbull, G., Fredua‐Agyeman, R., Hollman, K. and Kaus, S. (2021) Characterization of clubroot (Plasmodiophora brassicae) from canola (Brassica napus) in the Peace Country of Alberta, Canada. Can. J. Plant Pathol., 43, 155–161. https://doi.org/10.1080/07060661.2020.1776931.
Summanwar, A., Farid, M., Basu, U., Kav, N. and Rahman, H. (2021) Comparative transcriptome analysis of canola carrying clubroot resistance from ‘Mendel’ or Rutabaga and the development of molecular markers. Physiol. Mol. Plant Pathol., 114, 101640. https://doi.org/10.1016/j.pmpp.2021.101640.
Sun, K., Hunt, K. and Hauser, B.A. (2004) Ovule abortion in Arabidopsis triggered by stress. Plant Physiol., 135, 2358–2367. https://doi.org/10.1104/pp.104.043091.
Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E. and Mittler, R. (2014) Abiotic and biotic stress combinations. New Phytol., 203, 32–43. https://doi.org/10.1111/nph.12797.
Tellmann G. (2006) The E‐Method: a highly accurate technique for gene‐expression analysis. Nat. Methods, 3. https://doi.org/10.1038/nmeth894.
ul Haq, S., Khan, A., Ali, M., Khattak, A.M., Gai, W.X., Zhang, H.X., Wei, A.M. and Gong, Z.H. (2019) Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int. J. Mol. Sci., 20, 5321. https://doi.org/10.3390/ijms20215321.
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real‐time quantitative RT‐PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3, research0034.1. https://doi.org/10.1186/gb-2002-3-7-research0034.
Verdier, J. and Thompson, R.D. (2008) Transcriptional regulation of storage protein synthesis during dicotyledon seed filling. Plant Cell Physiol., 49, 1263–1271. https://doi.org/10.1093/pcp/pcn116.
Wickham, H. (2009) Ggplot2 elegant graphics for data analysis 2nd edn. Springer, New York.
Wolfe, C.J., Kohane, I.S. and Butte, A.J. (2005) Systematic survey reveals general applicability of “guilt‐by‐association” within gene coexpression networks. BMC Bioinformatics, 6, 227. https://doi.org/10.1186/1471-2105-6-227.
Xu, P., Chen, F., Mannas, J.P., Feldman, T., Sumner, L.W. and Roossinck, M.J. (2008) Virus infection improves drought tolerance. New Phytol., 180, 911–921. https://doi.org/10.1111/j.1469-8137.2008.02627.x.
Yao, L., Cheng, X., Gu, Z., Huang, W., Li, S., Wang, L., Wang, Y.‐F., Xu, P., Ma, H. and Ge, X. (2018) The AWPM‐19 family protein OsPM1 mediates abscisic acid influx and drought response in rice. Plant Cell, 30, 1258–1276. https://doi.org/10.1105/tpc.17.00770.
Zhang, B. and Horvath, S. (2005) A general framework for weighted gene co‐expression network analysis. Stat. Appl. Genet. Mol. Biol., 4, Article17. https://doi.org/10.2202/1544-6115.1128.

INRAE-BAP-IB2017-SQUAL Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement; Région Bretagne; ANR-14-JFAC-007-01 Agence Nationale de la Recherche

0 (Plant Proteins)

Date Created: 20240606 Date Completed: 20240606 Latest Revision: 20240606

20240606

10.1111/ppl.14130

38842416