CRISPR/Cas9-mediated mutations of FANTASTIC FOUR gene family for creating early flowering mutants in tomato.
CRISPR/Cas9
FANTASTIC FOUR
early flowering
germplasms
tomato
Journal
Plant biotechnology journal
ISSN: 1467-7652
Titre abrégé: Plant Biotechnol J
Pays: England
ID NLM: 101201889
Informations de publication
Date de publication:
09 Nov 2023
09 Nov 2023
Historique:
revised:
04
11
2023
received:
17
10
2022
accepted:
21
10
2023
medline:
9
11
2023
pubmed:
9
11
2023
entrez:
9
11
2023
Statut:
aheadofprint
Résumé
Flowering time is of great agricultural importance and the timing and extent of flowering usually determines yield and availability of flowers, fruits and seeds. Identification of genes determining flowering has important practical applications for tomato breeding. Here we demonstrate the roles of the FANTASTIC FOUR (FAF) gene family in regulating tomato flowering time. In this plant-specific gene family, SlFAF1/2a shows a constitutive expression pattern during the transition of the shoot apical meristem (SAM) from vegetative to reproductive growth and significantly influences flowering time. Overexpressing SlFAF1/2a causes earlier flowering compared with the transformations of other genes in the FAF family. SlFAF1/2c also positively regulates tomato flowering, although to a lesser extent. The other members of the SlFAF gene family, SlFAF1/2b, SlFAF3/4a and SlFAF3/4b, are negative regulators of tomato flowering and faf1/2b, faf3/4a and faf3/4b single mutants all display early flowering. We generated a series of early flowering mutants using the CRISPR/Cas9 editing system, and the faf1/2b faf3/4a faf3/4b triple mutant flowering earliest compared with other mutants. More importantly, these mutants show no adverse effect on yield. Our results have uncovered the role of the FAF gene family in regulating tomato flowering time and generated early flowering germplasms for molecular breeding.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fundamental Research Funds for the Central Universities
ID : 2662022YLPY001
Organisme : Hubei Key Research & Development Plan
ID : 2022BBA0062
Organisme : Hubei Key Research & Development Plan
ID : 2022BBA0066
Organisme : Key Project of Hubei Hongshan Laboratory
ID : 2021hszd007
Organisme : National Key Research & Development Plan
ID : 2021YFD1200201
Organisme : National Key Research & Development Plan
ID : 2022YFD1200502
Organisme : National Natural Science Foundation of China
ID : 32372696
Organisme : National Natural Science Foundation of China
ID : 31972426
Organisme : National Natural Science Foundation of China
ID : 31991182
Organisme : Wuhan Biological Breeding Major Project
ID : 2022021302024852
Organisme : HZAU-AGIS Cooperation Fund
ID : SZYJY2023022
Informations de copyright
© 2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
Références
An, H., Roussot, C., Suárez-López, P., Corbesier, L., Vincent, C., Piñeiro, M., Hepworth, S. et al. (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131, 3615-3626.
Andrés, F. and Coupland, G. (2012) The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639.
Benlloch, R., Berbel, A., Serrano-Mislata, A. and Madueño, F. (2007) Floral initiation and inflorescence architecture: a comparative view. Ann. Bot. 100, 659-676.
Bhargava, A., Clabaugh, I., To, J.P., Maxwell, B.B., Chiang, Y.H., Schaller, G.E., Loraine, A. et al. (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 162, 272-294.
Chailakhyan, M.K. (1936) New facts supporting the hormonal theory of plant development. Dokl. Akad. Nauk SSSR 4, 77-81.
Dielen, V., Quinet, M., Chao, J., Batoko, H., Havelange, A. and Kinet, J.M. (2004) UNIFLORA, a pivotal gene that regulates floral transition and meristem identity in tomato (Lycopersicon esculentum). New Phytol. 161, 393-400.
Garner, W.W. and Allard, H.A. (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J. Agric. Res. 18, 553-606.
Garner, W.W. and Allard, H.A. (1923) Further studies on photoperiodism, the response of plants to relative length of day and night. J. Agric. Res. 23, 871-920.
Kobayashi, Y. and Weigel, D. (2007) Move on up, it's time for change-mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21, 2371-2384.
Kumar, S., Stecher, G. and Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
Kwiatkowska, D. (2008) Flowering and apical meristem growth dynamics. J. Exp. Bot. 59, 187-201.
Lifschitz, E. and Eshed, Y. (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. J. Exp. Bot. 57, 3405-3414.
Lifschitz, E., Eviatar, T., Rozman, A., Shalit, A., Goldshmidt, A., Amsellem, Z., Paul Alvarez, J. et al. (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. 103, 6398-6403.
Lippman, Z.B., Cohen, O., Alvarez, J.P., Abu-Abied, M., Pekker, I., Paran, I., Eshed, Y. et al. (2008) The making of a compound inflorescence in tomato and related nightshades. PLoS Biol. 6, e288.
MacAlister, C.A., Park, S.J., Jiang, K., Marcel, F., Bendahmane, A., Izkovich, Y., Eshed, Y. et al. (2012) Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene. Nat. Genet. 44, 1393-1398.
Mauxion, J.P., Chevalier, C. and Gonzalez, N. (2021) Complex cellular and molecular events determining fruit size. Trends Plant Sci. 26, 1023-1038.
Meir, Z., Aviezer, I., Chongloi, G.L., Ben-Kiki, O., Bronstein, R., Mukamel, Z., Keren-Shaul, H. et al. (2021) Dissection of floral transition by single-meristem transcriptomes at high temporal resolution. Nat. Plants 7, 800-813.
Molinero-Rosales, N., Jamilena, M., Zurita, S., Gómez, P., Capel, J. and Lozano, R. (1999) FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J. 20, 685-693.
Molinero-Rosales, N., Latorre, A., Jamilena, M. and Lozano, R. (2004) SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta 218, 427-434.
Mu, Q., Huang, Z., Chakrabarti, M., Illa-Berenguer, E., Liu, X., Wang, Y., Ramos, A. et al. (2017) Fruit weight is controlled by Cell Size Regulator encoding a novel protein that is expressed in maturing tomato fruits. PLoS Genet. 13, e1006930.
Muller, D., Waldie, T., Miyawaki, K., To, J.P., Melnyk, C.W., Kieber, J.J., Kakimoto, T. et al. (2015) Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant J. 82, 874-886.
Ouyang, B., Chen, Y., Li, H., Qian, C., Huang, S. and Ye, Z. (2005) Transformation of tomatoes with osmotin and chitinase genes and their resistance to Fusarium wilt. J. Hortic Sci. Biotech. 80, 517-522.
Park, S.J., Jiang, K., Schatz, M.C. and Lippman, Z.B. (2011) Rate of meristem maturation determines inflorescence architecture in tomato. Proc. Natl. Acad. Sci. 109, 639-644.
Pnueli, L., Carmel-Goren, L., Hareven, D., Gutfinger, T., Alvarez, J., Ganal, M., Zamir, D. et al. (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125, 1979-1989.
Reinhart, B.J., Liu, T., Newell, N.R., Magnani, E., Huang, T., Kerstetter, R., Michaels, S. et al. (2013) Establishing a framework for the Ad/abaxial regulatory network of Arabidopsis: ascertaining targets of class III homeodomain leucine zipper and KANADI regulation. Plant Cell 25, 3228-3249.
Schmid, M., Uhlenhaut, N.H., Godard, F., Demar, M., Bressan, R., Weigel, D. and Lohmann, J.U. (2003) Dissection of floral induction pathways using global expression analysis. Development 130, 6001-6012.
Soyk, S., Muller, N.A., Park, S.J., Schmalenbach, I., Jiang, K., Hayama, R., Zhang, L. et al. (2017) Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat. Genet. 49, 162-168.
Szymkowiak, E.J. and Irish, E.E. (2006) JOINTLESS suppresses sympodial identity in inflorescence meristems of tomato. Planta 223, 646-658.
Torti, S., Fornara, F., Vincent, C., Andres, F., Nordstrom, K., Gobel, U., Knoll, D. et al. (2012) Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24, 444-462.
Turck, F., Fornara, F. and Coupland, G. (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573-594.
Wahl, V., Brand, L.H., Guo, Y. and Schmid, M. (2010) The FANTASTIC FOUR proteins influence shoot meristem size in Arabidopsis thaliana. BMC Plant Biol. 10, 285.
Weberling, F. (1992) Morphology of Flowers and Inflorescences. Cambridge, UK: Cambridge University Press.
Xie, K., Minkenberg, B. and Yang, Y. (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. USA 112, 3570-3575.
Zhang, T., Wang, Y., Munir, S., Wang, T., Ye, Z., Zhang, J. and Zhang, Y. (2022) Cyclin gene SlCycB1;2 alters plant architecture in association with histone H3.2 in tomato. Hortic. Plant J. 8, 341-350.