AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Horticultural Plant Journal Article
PDF (4.8 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper

Ectopic expression of VvFUS3, B3-domain transcription factor, in tomato influences seed development via affecting endoreduplication and hormones

Bilal Ahmada,b,1, Songlin Zhanga,b,1, Jin Yaoa,b, Shengyue Chaia,b, Vivek Yadavb, Habib-ur-Rehman Atharc, Mati Ur Rahmand, Li Wange, Xiping Wanga,b( )
State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A & F University, Yangling, Shaanxi 712100, China
Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A & F University, Yangling, Shaanxi 712100, China
Institute of Pure and Applied Biology, Bahauddin Zakariya University, Multan 60800, Pakistan
College of Food Engineering and Nutritional Science, Shaanxi Normal University, Xi'an 710119, China
College of Horticulture, Hebei Agricultural University, Baoding, Hebei 071000, China

1 These authors contributed equally to this work.

Show Author Information

Abstract

FUSCA3 (FUS3) is a member of B3-domain transcription factor family and master regulator of seed development. It has potential roles in hormone biosynthesis and signaling pathways and therefore plays diverse roles in plant life cycle, especially in seed germination, dormancy, embryo formation, seed and fruit development, and maturation. However, there is limited information about its functions in seed and fruit development of grapevine. In this study, we expressed VvFUS3 in tomato for its functional characterization. Overexpression of VvFUS3 in tomato led to a reduction in seed number and seed weight without affecting the fruit size. Histological analysis found that both cell expansion and cell division in transgenic seed and fruit pericarp have been affected. However, there were no obvious differences in pollen size, shape, and viability, suggesting that VvFUS3 affects seed development but not the pollen grains. Moreover, the expression of several genes with presumed roles in seed development and hormone signaling pathways was also influenced by VvFUS3. These results suggest that VvFUS3 is involved in hormonal signaling pathways that regulate seed number and size. In conclusion, our study provides novel preliminary information about the pivotal roles of VvFUS3 in seed and fruit development and these findings can potentially serve as a reference for molecular breeding of seedless grapes.

Keywords

Vitis vinifera L.HormoneABI3B3 transcription factorSeed numberEndoreduplication

References

 

Ahmad, B., Yao, J., Zhang, S., Li, X., Zhang, X., Yadav, V., Wang, X., 2020. Genome-wide characterization and expression profiling of GASA Genes during different stages of seed development in grapevine (Vitis vinifera L.) predict their involvement in seed development. Int J Mol Sci, 21: 1088.
Crossref Google Scholar
 

Alpert, K.B., Grandillo, S., Tanksley, S.D., 1995. fw 2.2: a major QTL controlling fruit weight is common to both red- and green-fruited tomato species. Theor Appl Genet, 91: 994–1000.
Crossref Google Scholar
 

Bou-Torrent, J., Martínez-García, J.F., García-Martínez, J.L., Prat, S., 2011. Gibberellin A1 metabolism contributes to the control of photoperiod-mediated tuberization in potato. PLoS ONE, 6: e24458.
Crossref Google Scholar
 

Braybrook, S.A., Stone, S.L., Park, S., Bui, A.Q., Le, B.H., Fischer, R.L., Goldberg, R.B., Harada, J.J., 2006. Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci U S A, 103: 3468–3473.
Crossref Google Scholar
 

Breitel, D.A., Chappell-Maor, L., Meir, S., Panizel, I., Aharoni, A., 2016. Auxin response factor 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS Genet, 12: e1005903.
Crossref Google Scholar
 

Brocard-Gifford, I.M., Lynch, T.J., Finkelstein, R.R., 2003. Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol, 131: 78–92.
Crossref Google Scholar
 

Carbonero, P., Iglesias-Fernández, R., Vicente-Carbajosa, J., 2016. The AFL subfamily of B3 transcription factors: evolution and function in angiosperm seeds. J Exp Bot, 68: 871–880.
Crossref Google Scholar
 

Chakrabarti, M., Zhang, N., Sauvage, C., 2013. A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci U S A, 110: 17125–17130.
Crossref Google Scholar
 

Chan, A., Carianopol, C., Tsai, A.Y., Varatharajah, K., Chiu, R.S., Gazzarrini, S., 2017. SnRK1 phosphorylation of FUSCA3 positively regulates embryogenesis, seed yield, and plant growth at high temperature in Arabidopsis. J Exp Bot, 68: 4219–4231.
Crossref Google Scholar
 

Chen, M., Zhang, B., Li, C., Kulaveerasingam, Harikrishna, Chew, Fook, T, Yu, 2015. Transparent Testa GLABRA1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiol, 169: 391–402.
Crossref Google Scholar
 

Chhun, T., Chong, S., Park, B., Wong, E., Yin, J., Kim, M., Chua, N., 2016. HSI2 repressor recruits MED13 and HDA6 to down-regulate seed maturation gene expression directly during Arabidopsis early seedling growth. Plant Cell Physiol, 57: 1689–1706.
Crossref Google Scholar
 

Chiu, R.S., Nahal, H., Provart, N.J., Gazzarrini, S., 2012. The role of the Arabidopsis FUSCA3 transcription factor during inhibition of seed germination at high temperature. BMC Plant Biol, 12: 15.
Crossref Google Scholar
 

Curaba, J., Moritz, T., Blervaque, R., Parcy, F., Raz, V., Herzog, M., 2004. AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol, 136: 3660–3669.
Crossref Google Scholar
 

Czerednik, A., Busscher, M., Angenent, G.C., de Maagd, R.A., 2015. The cell size distribution of tomato fruit can be changed by overexpression of CDKA1. Plant Biotechnol J, 13: 259–268.
Crossref Google Scholar
 

Fatihi, A., Boulard, C., Bouyer, D., Baud, S., Dubreucq, B., 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.
Crossref Google Scholar
 

García-Hurtado, N., Carrerasup, E., Ruiz-Rivero, O., López-Gresa, M., Heddensup, P., Gongsup, F., José Luis García-Martínez, J., 2012. The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. J Exp Bot, 63: 5803–5813.
Crossref Google Scholar
 

Gazzarrini, S., Tsuchiya, Y., Lumba, S., Okamoto, M., McCourt, P., 2004. The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell, 7: 373–385.
Crossref Google Scholar
 

Gonzalez, N., Gévaudant, F., Hernould, M., Chevalier, C., Mouras, A., 2007. The cell cycle-associated protein kinase WEE1 regulates cell size in relation to endoreduplication in developing tomato fruit. Plant J, 51: 642–655.
Crossref Google Scholar
 

Gonzalez, N., Hernould, M., Delmas, F., Gévaudant, F., Duffe, P., Causse, M., 2004. Molecular characterization of a WEE1 gene homologue in tomato (Lycopersicon esculentum Mill.). Plant Mol Biol, 56: 849–861.
Crossref Google Scholar
 

Heslop-Harrison, J., Heslop-Harrison, Y., 1970. Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technol, 45: 115–120.
Crossref Google Scholar
 

Holdsworth, M.J., Bentsink, L., Soppe, W.J., 2008. Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol, 179: 33–54.
Crossref Google Scholar
 

Horton, P., Park, K., Obayashi, T., Fujita, N., Harada, H., Admas-Colier, C.J., Nakai, K., 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Res, 35: W585-W587.
Crossref Google Scholar
 

Huang, L., Yin, X., Sun, X., Yang, J., Rahman, M., Chen, Z., Wang, X., 2018. Expression of a grape VqSTS36-Increased resistance to powdery mildew and osmotic stress in Arabidopsis but enhanced susceptibility to Botrytis cinerea in Arabidopsis and tomato. Int J Mol Sci, 19: 2985.
Crossref Google Scholar
 

Joubès, J., Chevalier, C., Dudits, D., Heberle-Bors, E., 2000. CDK-related protein kinases in plants. Plant Mol Biol, 43: 607–620.
Crossref Google Scholar
 

Kagaya, Y., Toyoshima, R., Okuda, R., Usui, H., Yamamoto, A., Hattori, T., 2005. Leafy Cotyledon1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC acid insensitive3. Plant Cell Physiol, 46: 399–406.
Crossref Google Scholar
 

Keith, K., Kraml, M., Dengler, N.G., McCourt, P., 1994. FUSCA3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell, 6: 589–600.
Crossref Google Scholar
 

Kroj, T., Savino, G., Valon, C., Giraudat, J., Parcy, F., 2003. Regulation of storage protein gene expression in Arabidopsis. Development, 130: 6065–6073.
Crossref Google Scholar
 

Lepiniec, L., Devic, M., Roscoe, T.J., Bouyer, D., Zhou, D.X., Boulard, C., 2018. Molecular and epigenetic regulations and functions of the LAFL transcriptional regulators that control seed development. Plant Reprod, 31: 291–307.
Crossref Google Scholar
 

Lumba, S., Tsuchiya, Y., Delmas, F., Hezky, J., Provart, N.J., Lu, Q.S., 2012. The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol, 10: 8.
Crossref Google Scholar
 

Matsuo, S., Kikuchi, K., Fukuda, M., Honda, I., Imanishi, S., 2012. Roles and regulation of cytokinins in tomato fruit development. J Exp Bot, 63: 5569–5579.
Crossref Google Scholar
 

Mizukami, Y., 2001. A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol, 4: 533–539.
Crossref Google Scholar
 

Mu, J., Tan, H., Qi, Z., Fu, F., Yan, L., 2008. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol, 148: 1042–1054.
Crossref Google Scholar
 

Pattison, R.J., Csukasi, F., Catalá, C., 2014. Mechanisms regulating auxin action during fruit development. Physiol Plant, 151: 62–72.
Crossref Google Scholar
 

Pelletier, J.M., Kwong, R.W., Park, S., Le, B.H., Harada, J.J., 2017. LEC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc Natl Acad Sci U S A, 114: E6710-E6719.
Crossref Google Scholar
 

Righetti, K., Vu, J.L., Pelletier, S., Vu, B.L., Buitink, J., 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.
Crossref Google Scholar
 

Roscoe, T.T., Guilleminot, J., Bessoule, J.J., Berger, F., Devic, M., 2015. Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol, 56: 1215–1228.
Crossref Google Scholar
 

Royo, C., Torres-Perez, R., Mauri, N., 2018. The major origin of seedless grapes is associated with a missense mutation in the MADS-box gene VviAGL11. Plant Physiol, 177: 1234–1253.
Crossref Google Scholar
 

Santos-Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Lepiniec, L., 2008. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J, 54: 608–620.
Crossref Google Scholar
 

Schmittgen, T.D., Livak, K.J., 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc, 3: 1101–1108.
Crossref Google Scholar
 

Sreenivasulu, N., Wobus, U., 2013. Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol, 64: 189–217.
Crossref Google Scholar
 

Stone, S.L., Braybrook, S.A., Paula, S.L., Kwong, L.W., Meuser, J., Pelletier, J., 2008. Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci U S A, 105: 3151–3156.
Crossref Google Scholar
 

Sun, X., Zhang, S., Li, X., Zhang, X., Wang, X., 2020. A Mads-box transcription factor from grapevine, VvMADS45, influences seed development. Tissue Organ Cult, 141: 105–118. Plant Cell.
Crossref Google Scholar
 

Tang, L.P., Zhou, C., Wang, S.S., Yuan, J., Zhang, X.S., Sun, Y.H., 2017. FUSCA3 interacting with LEAFY COTYLEDON2 controls lateral root formation through regulating YUCCA4 gene expression in Arabidopsis thaliana. New Phytol, 213: 1740–1754.
Crossref Google Scholar
 

Vicient, C.M., Bies-Etheve, N., Delseny, M., 2000. Changes in gene expression in the leafy cotyledon1 (LEC1) and FUSCA3 (FUS3) mutants of Arabidopsis thaliana. J Exp Bot, 51: 995–1003.
Crossref Google Scholar
 

Wan, S., Li, W., Zhu, Y., Liu, Z., Zhan, J., 2014. Genome-wide identification, characterization and expression analysis of the auxin response factor gene family in Vitis vinifera. Plant Cell Rep, 33: 1365–1375.
Crossref Google Scholar
 

Wang, F., Perry, S.E., 2013. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol, 161: 1251–1264.
Crossref Google Scholar
 

Wang, L., Hu, X., Jiao, C., Li, Z., Fei, Z., Yan, X., Liu, C., Wang, Y., Wang, X., 2016. Transcriptome analyses of seed development in grape hybrids reveals a possible mechanism influencing seed size. BMC Genom, 17: 898.
Crossref Google Scholar
 

Yamasaki, Y., Gao, F., Jordan, M.C., Ayele, B.T., 2017. Seed maturation associated transcriptional programs and regulatory networks underlying genotypic difference in seed dormancy and size/weight in wheat (Triticum aestivum L.). BMC Plant Biol, 17: 154.
Crossref Google Scholar
 

Zhang, C., Fan, X.C., Liu, C.H., Fang, J. G, 2021. Anatomical berry characteristics during the development of grape berries with different shapes. Hortic Plant J, 7: 295–306.
Crossref Google Scholar
 

Zheng, Q., Zheng, Y., Ji, H., Burnie, W., Perry, S.E., 2016. Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiol, 172: 2374–2387.
Crossref Google Scholar
 

Zheng, Y., Ren, N., Wang, H., Stromberg, A.J., Perry, S.E., 2009. Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell, 21: 2563–2577.
Crossref Google Scholar
Horticultural Plant Journal
Volume 8 Issue 3,
May 2022
Pages 351-360
DOI: 10.1016/j.hpj.2020.12.009
Cite this article:
Ahmad B, Zhang S, Yao J, et al. Ectopic expression of VvFUS3, B3-domain transcription factor, in tomato influences seed development via affecting endoreduplication and hormones. Horticultural Plant Journal, 2022, 8(3): 351-360. https://doi.org/10.1016/j.hpj.2020.12.009

336

Views

9

Downloads

12

Crossref

9

Web of Science

11

Scopus

0

CSCD

Altmetrics
Received: 25 November 2020
Revised: 23 December 2020
Accepted: 27 May 2021
Published: 26 June 2021
© 2021 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Return