Abstract
Main conclusion
Overexpression of JcSEUSS1 resulted in late flowering, reduced flower number, wrinkled kernels, and decreased seed yield in Jatopha curcas, while downregulation of JcSEUSS1 increased flower number and seed production.
Abstract
The seed oil of Jatropha curcas is suitable as an ideal alternative for diesel fuel, yet the seed yield of Jatropha is restricted by its small number of female flowers and low seed setting rate. Therefore, it is crucial to identify genes that regulate flowering and seed set, and hence improve seed yield. In this study, overexpression of JcSEUSS1 resulted in late flowering, fewer flowers and fruits, and smaller fruits and seeds, causing reduced seed production and oil content. In contrast, the downregulation of JcSEUSS1 by RNA interference (RNAi) technology caused an increase in the flower number and seed yield. However, the flowering time, seed number per fruit, seed weight, and size exhibited no obvious changes in JcSEUSS1-RNAi plants. Moreover, the fatty acid composition also changed in JcSEUSS1 overexpression and RNAi plants, the percentage of unsaturated fatty acids (FAs) was increased in overexpression plants, and the saturated FAs were increased in RNAi plants. These results indicate that JcSEUSS1 played a negative role in regulating reproductive growth and worked redundantly with other genes in the regulation of flowering time, seed number per fruit, seed weight, and size.
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Data availability
No new sequence data were published in the present paper. Sequence data included in the paper can be obtained from the publicly available genome of Jatropha curcas (https://www.ncbi.nlm.nih.gov/bioproject/38697) under the following accession numbers: JcSEUSS1 (XM_012211182) and JcACTIN1 (NM_112764).
Abbreviations
- SEU :
-
SEUSS
- RNAi:
-
RNA interference
- FA:
-
Fatty acid
- GA:
-
Gibberellin
- JcGA20ox :
-
Jatropha curcas GA 20-oxidase
References
Akashi K (2012) Jatropha research: a new frontier for biofuel development. Plant Biotechnol 29(2):121–189. https://doi.org/10.5511/plantbiotechnolog.12.0003P
Alherbawi M, McKay G, Mackey HR, Al-Ansari T (2021) Jatropha curcas for jet biofuel production: Current status and future prospects. Renew Sust Energ Rev 135:110396. https://doi.org/10.1016/j.rser.2020.110396
Ali S, Fazal T, Javed F, Hafeez A, Akhtar M, Haider B, Saif ur Rehman M, Zimmerman WB, Rehman F (2020) Investigating biodiesel production strategies as a sustainable energy resource for Pakistan. J Clean Prod 259:120729. https://doi.org/10.1016/j.jclepro.2020.120729
Augustus GDPS, Jayabalan M, Seiler GJ (2002) Evaluation and bioinduction of energy components of Jatropha curcas. Biomass Bioenergy 23(3):161–164. https://doi.org/10.1016/S0961-9534(02)00044-2
Azhakanandam S, Nole-Wilson S, Bao F, Franks RG (2008) SEUSS and AINTEGUMENTA mediate patterning and ovule initiation during gynoecium medial domain development. Plant Physiol 146(3):1165–1181. https://doi.org/10.1104/pp.107.114751
Bao F, Azhakanandam S, Franks RG (2010) SEUSS and SEUSS-LIKE transcriptional adaptors regulate floral and embryonic development in Arabidopsis. Plant Physiol 152(2):821–836. https://doi.org/10.1104/pp.109.146183
Bowman JL, Drews GN, Meyerowitz EM (1991) Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell 3(8):749–758. https://doi.org/10.1105/tpc.3.8.749
Cai Y, Sun D, Wu G, Peng J (2010) ISSR-based genetic diversity of Jatropha curcas germplasm in China. Biomass Bioenergy 34(12):1739–1750. https://doi.org/10.1016/j.biombioe.2010.07.001
Callegari A, Bolognesi S, Cecconet D, Capodaglio AG (2019) Production technologies, current role, and future prospects of biofuels feedstocks: a state-of-the-art review. Crit Rev Environ Sci Technol 50:384–436. https://doi.org/10.1080/10643389.2019.1629801
Ding LW, Sun QY, Wang ZY, Sun YB, Xu ZF (2008) Using silica particles to isolate total RNA from plant tissues recalcitrant to extraction in guanidine thiocyanate. Anal Biochem 374(2):426–428. https://doi.org/10.1016/j.ab.2007.11.030
Divakara BN, Upadhyaya HD, Wani SP, Gowda CLL (2010) Biology and genetic improvement of Jatropha curcas L.: a review. Appl Energy 87(3):732–742. https://doi.org/10.1016/j.apenergy.2009.07.013
Franks RG, Wang C, Levin JZ, Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129(1):253–263. https://doi.org/10.1242/dev.129.1.253
Franks RG, Liu Z, Fischer RL (2006) SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals. Planta 224(4):801–811. https://doi.org/10.1007/s00425-006-0264-6
Fu Q, Li C, Tang M, Tao YB, Pan BZ, Zhang L, Niu L, He H, Wang X, Xu ZF (2015) An efficient protocol for Agrobacterium-mediated transformation of the biofuel plant Jatropha curcas by optimizing kanamycin concentration and duration of delayed selection. Plant Biotechnol Rep 9(6):405–416. https://doi.org/10.1007/s11816-015-0377-0
Gong X, Flores-Vergara MA, Hong JH, Chu H, Lim J, Franks RG, Liu Z, Xu J (2016) SEUSS integrates gibberellin signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate middle cortex formation in the Arabidopsis root. Plant Physiol 170(3):1675–1683. https://doi.org/10.1104/pp.15.01501
Grigorova B, Mara C, Hollender C, Sijacic P, Chen X, Liu Z (2011) LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138(12):2451–2456. https://doi.org/10.1242/dev.058362
Guan HL, Huang BB, Chen MY, Wang XM, Song SW, Liu HC, Chen RY, Hao YW (2018) Genome-wide identification, phylogeny analysis, expression profiling, and determination of protein-protein interactions of the LEUNIG gene family members in tomato. Gene 679:1–10. https://doi.org/10.1016/j.gene.2018.08.075
Hartmann U, Hohmann U, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360. https://doi.org/10.1046/j.1365-313x.2000.00682.x
Hu Y-X, Hu Y-X, Tao Y-B, Xu Z-F (2017) Overexpression of Jatropha Gibberellin 2-oxidase 6 (JcGA2ox6) induces dwarfism and smaller leaves, flowers and fruits in Arabidopsis and Jatropha. Front Plant Sci 8:2103. https://doi.org/10.3389/fpls.2017.02103
Jack T, Fox GL, Meyerowitz EM (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76(4):703–716. https://doi.org/10.1016/0092-8674(94)90509-6
Jiang X, Lubini G, Hernandes-Lopes J, Rijnsburger K, Veltkamp V, de Maagd RA, Angenent GC, Bemer M (2022) FRUITFULL-like genes regulate flowering time and inflorescence architecture in tomato. Plant Cell 34(3):1002–1019. https://doi.org/10.1093/plcell/koab298
Jonas M, Ketlogetswe C, Gandure J (2020) Variation of Jatropha curcas seed oil content and fatty acid composition with fruit maturity stage. Heliyon 6(1):e03285. https://doi.org/10.1016/j.heliyon.2020.e03285
Kazamia E, Smith AG (2014) Assessing the environmental sustainability of biofuels. Trends Plant Sci 19(10):615–618. https://doi.org/10.1016/j.tplants.2014.08.001
Khalil HPSA, Aprilia NAS, Bhat AH, Jawaid M, Paridah MT, Rudi D (2013) A Jatropha biomass as renewable materials for biocomposites and its applications. Renew Sust Energ Rev 22:667–685. https://doi.org/10.1016/j.rser.2012.12.036
Kumar A, Sharma S (2008) An evaluation of multipurpose oil seed crop for industrial uses (Jatropha curcas L.): a review. Ind Crops Prod 28(1):1–10. https://doi.org/10.1016/j.indcrop.2008.01.001
Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254. https://doi.org/10.1093/jxb/erq098
Li CQ, Luo L, Fu QT, Niu LJ, Xu ZF (2014) Isolation and functional characterization of JcFT, a FLOWERING LOCUS T (FT) homologous gene from the biofuel plant Jatropha curcas. BMC Plant Biol 14:125. https://doi.org/10.1186/1471-2229-14-125
Li CQ, Fu QT, Niu LJ, Luo L, Chen JH, Xu ZF (2017) Three TFL1 homologues regulate floral initiation in the biofuel plant Jatropha curcas. Sci Rep 7:43090. https://doi.org/10.1038/srep43090
Mardhiah HH, Ong HC, Masjuki HH, Lim S, Pang YL (2017) Investigation of carbon-based solid acid catalyst from Jatropha curcas biomass in biodiesel production. Energy Convers Manag 144:10–17. https://doi.org/10.1016/j.enconman.2017.04.038
Marriott PE, Gómez LD, McQueen-Mason SJ (2016) Unlocking the potential of lignocellulosic biomass through plant science. New Phytol 209(4):1366–1381. https://doi.org/10.1111/nph.13684
Mofijur M, Rasul MG, Hyde J, Azad AK, Mamat R, Bhuiya MMK (2016) Role of biofuel and their binary (diesel–biodiesel) and ternary (ethanol–biodiesel–diesel) blends on internal combustion engines emission reduction. Renew Sust Energ Rev 53:265–278. https://doi.org/10.1016/j.rser.2015.08.046
Nole-Wilson S, Rueschhoff EE, Bhatti H, Franks RG (2010) Synergistic disruptions in seuss cyp85A2 double mutants reveal a role for brassinolide synthesis during gynoecium and ovule development. BMC Plant Biol 10:198. https://doi.org/10.1186/1471-2229-10-198
Pan B-Z, Xu Z-F (2011) Benzyladenine treatment significantly increases the seed yield of the biofuel plant Jatropha curcas. J Plant Growth Regul 30(2):166–174. https://doi.org/10.1007/s00344-010-9179-3
Pandey VC, Singh K, Singh JS, Kumar A, Singh B, Singh RP (2012) Jatropha curcas: a potential biofuel plant for sustainable environmental development. Renew Sust Energ Rev 16(5):2870–2883. https://doi.org/10.1016/j.rser.2012.02.004
Pfluger J, Zambryski P (2004) The role of SEUSS in auxin response and floral organ patterning. Development 131(19):4697–4707. https://doi.org/10.1242/dev.01306
Pua F-l, Fang Z, Zakaria S, Guo F, Chia C-h (2011) Direct production of biodiesel from high-acid value Jatrophaoil with solid acid catalyst derived from lignin. Biotechnol Biofuels 4(1):56. https://doi.org/10.1186/1754-6834-4-56
Sridhar VV, Surendrarao A, Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133(16):3159–3166. https://doi.org/10.1242/dev.02498
Sun Y, Wang C, Wang N, Jiang X, Mao H, Zhu C, Wen F, Wang X, Lu Z, Yue G, Xu Z, Ye J (2017) Manipulation of Auxin Response Factor 19 affects seed size in the woody perennial Jatropha curcas. Sci Rep 7:40844. https://doi.org/10.1038/srep40844
Tanaka W, Toriba T, Hirano HY (2017) Three TOB1-related YABBY genes are required to maintain proper function of the spikelet and branch meristems in rice. New Phytol 215(2):825–839. https://doi.org/10.1111/nph.14617
Tang M, Tao YB, Fu Q, Song Y, Niu L, Xu ZF (2016a) An ortholog of LEAFY in Jatropha curcas regulates flowering time and floral organ development. Sci Rep 6:37306. https://doi.org/10.1038/srep37306
Tang M, Tao YB, Xu ZF (2016) Ectopic expression of Jatropha curcas APETALA1 (JcAP1) caused early flowering in Arabidopsis, but not in Jatropha. PeerJ 4:e1969. https://doi.org/10.7717/peerj.1969
Tang M, Bai X, Wang J, Chen T, Meng X, Deng H, Li C, Xu Z-F (2022) Efficiency of graft-transmitted JcFT for floral induction in woody perennial species of the Jatropha genus depends on transport distance. Tree Physiol 42(1):189–201. https://doi.org/10.1093/treephys/tpab116
Tatikonda L, Wani SP, Kannan S, Beerelli N, Sreedevi TK, Hoisington DA, Devi P, Varshney RK (2009) AFLP-based molecular characterization of an elite germplasm collection of Jatropha curcas L., a biofuel plant. Plant Sci 176(4):505–513. https://doi.org/10.1016/j.plantsci.2009.01.006
Wang J, Ming X, Tao Y, Tang M, Xu Z (2020) Over-expression of JcSEUSS1 from Jatropha curcas induce the accumulation of anthocyanin in leaves. Mol Plant Breeding 19(23):7851–7860. https://doi.org/10.13271/j.mpb.019.007851
Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Mol Plant 8(7):983–997. https://doi.org/10.1016/j.molp.2015.01.007
Wu J-Q, Liu Y, Tang L, Zhang F-L, Chen F (2011) A study on structural features in early flower development of Jatropha curcas L. and the classification of its inflorescences. Afr J Agri Res 6:275–284. https://doi.org/10.5897/AJAR09.727
Wynn AN, Seaman AA, Jones AL, Franks RG (2014) Novel functional roles for PERIANTHIA and SEUSS during floral organ identity specification, floral meristem termination, and gynoecial development. Front Plant Sci 5:130. https://doi.org/10.3389/fpls.2014.00130
Yang C, Liu X, Li D, Zhu X, Wei Z, Feng Z, Zhang L, He J, Mou C, Jiang L, Wan J (2019) OsLUGL is involved in the regulating auxin level and OsARFs expression in rice (Oryza sativa L.). Plant Sci 288:110239. https://doi.org/10.1016/j.plantsci.2019.110239
Ye J, Wang C, Sun Y, Qu J, Mao H, Chua NH (2018) Overexpression of a transcription factor increases lipid content in a woody perennial Jatropha curcas. Front Plant Sci 9:1479. https://doi.org/10.3389/fpls.2018.01479
Zhai H, Zhang X, You Y, Lin L, Zhou W, Li C (2020) SEUSS integrates transcriptional and epigenetic control of root stem cell organizer specification. EMBO J 39(20):e105047. https://doi.org/10.15252/embj.2020105047
Zhang TT, He HY, Xu CJ, Fu QT, Tao YB, Xu RH, Xu ZF (2021) Overexpression of type 1 and 2 diacylglycerol acyltransferase genes (JcDGAT1 and JcDGAT2) enhances oil production in the woody perennial biofuel plant Jatropha curcas. Plants. https://doi.org/10.3390/plants10040699
Acknowledgements
We thank Lixiu Ding, Jie Yang, Yuan Wu, and Chuanjia Xu for helping transplant the transgenic Jatropha seedlings. The authors gratefully acknowledge the Central Laboratory of the Xishuangbanna Tropical Botanical Garden (XTBG) and the National Forest Ecosystem Research Station at Xishuangbanna for providing the research facilities.
Funding
This work was supported by the Natural Science Foundation of China (Grant number 32371836, 31700273), Yunnan Fundamental Research Projects (grant No. 202205AC160030, 2018FB060), and the Young Elite Scientists Sponsorship Program by the Chinese Society of Tropical Crops (Grant number CSTC-QN201701). The Natural Science Foundation of Guizhou Province (202142924832410240).
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JW performed the experiments, analyzed the data, and wrote the manuscript. XB performed the experiments, analyzed the data, and revised the manuscript. YS, HD, LC, and HH helped collect the data. XM, Y-BT, and Z-FX conceived the study and revised the manuscript. MT designed the experiment, conceived the study, and revised the manuscript. All authors reviewed and approved the final manuscript.
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Wang, J., Bai, X., Su, Y. et al. JcSEUSS1 negatively regulates reproductive organ development in perennial woody Jatropha curcas. Planta 258, 88 (2023). https://doi.org/10.1007/s00425-023-04244-7
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DOI: https://doi.org/10.1007/s00425-023-04244-7