Reassessing the contribution of TOMATO AGAMOUS-LIKE1 to fruit ripening by CRISPR/Cas9 mutagenesis.

CRISPR-Cas9 Fruit ripening Gene editing TOMATO AGAMOUS-LIKE 1 Tomato

Journal

Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970

Informations de publication

Date de publication:
22 Jan 2024
Historique:
received: 26 08 2023
accepted: 16 10 2023
medline: 22 1 2024
pubmed: 22 1 2024
entrez: 21 1 2024
Statut: epublish

Résumé

CRISPR/Cas9-edited TOMATO AGAMOUS-LIKE1 (TAGL1) provided new insights into fruit ripening. TOMATO AGAMOUS LIKE 1 (TAGL1) has been identified as playing a key role in the process of tomato fruit development and ripening. We have re-evaluated the functions of TAGL1 using CRISPR/Cas9 mutagenesis. Three KO mutants contained frameshift mutations resulting in premature termination codons due to a 1 bp insertion. TAGL1-KO mutants exhibited dark immature fruits and orange ripening fruits. The fruit shape was characterized by a prominent pointed tip at the end and the pericarp thickness was significantly thinner. TAGL1-KO mutants showed reduced ethylene biosynthesis, increased firmness, and delayed onset of ripening. The chlorophyll content of TAGL1-KO mutants was higher in the mature green stage and the lycopene content of TAGL1-KO mutants in the ripening stage was lower compared to the WT. ACS2, ACS4, ACO1, ACO3, PG2a, PL, PME, EXP1, and PSY1 in the mutants were significantly down-regulated during ripening. Ripening fruits in the double mutant of rin and tagl1 showed a more extreme phenotype than the rin mutant suggesting that the double mutation acts synergistically during ripening. TAGL1-targeted mutagenesis by CRISPR/Cas9 strengthens its regulatory functions controlling ripening parameters and provides new insights into fruit ripening.

Identifiants

pubmed: 38246942
doi: 10.1007/s00299-023-03105-7
pii: 10.1007/s00299-023-03105-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

41

Subventions

Organisme : National Research Foundation of Korea
ID : 2021R1A2C2093789

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Gao Y, Wei W, Fan Z, Zhao X, Zhang Y, Jing Y, Zhu B, Zhu H, Shan W, Chen J (2020) Re-evaluation of the nor mutation and the role of the NAC-NOR transcription factor in tomato fruit ripening. J Exp Bot 71:3560–3574
doi: 10.1093/jxb/eraa131 pubmed: 32338291 pmcid: 7307841
Güler Z, Şekerli YE (2013) Distribution of volatile compounds in organic tomato (lycopersicon esculentum) at different ripening stages. Akad Gıda 11:6–13
Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60:1081–1095
doi: 10.1111/j.1365-313X.2009.04064.x pubmed: 19891701
Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Shima Y, Nakamura N, Kotake-Nara E, Kawasaki S, Toki S (2017) Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nat Plants 3:866–874
doi: 10.1038/s41477-017-0041-5 pubmed: 29085071
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59
doi: 10.1146/annurev-genet-110410-132507 pubmed: 22060040
Lee JM, Joung JG, Mcquinn R, Chung MY, Fei Z, Tieman D, Klee H, Giovannoni J (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J 70:191–204
doi: 10.1111/j.1365-313X.2011.04863.x pubmed: 22111515
Liu G, Li C, Yu H, Tao P, Yuan L, Ye J, Chen W, Wang Y, Ge P, Zhang J, Zhou G, Zheng W, Ye Z, Zhang Y (2020) GREEN STRIPE, encoding methylated TOMATO AGAMOUS-LIKE 1, regulates chloroplast development and Chl synthesis in fruit. New Phytol 228:302–317
doi: 10.1111/nph.16705 pubmed: 32463946
Vrebalov J, Pan IL, Arroyo AJM, Mcquinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21:3041–3062
doi: 10.1105/tpc.109.066936 pubmed: 19880793 pmcid: 2782289
Wang R, Angenent GC, Seymour G, De Maagd RA (2020) Revisiting the role of master regulators in tomato ripening. Trends Plant Sci 25:291–301
doi: 10.1016/j.tplants.2019.11.005 pubmed: 31926765
Yoo HJ, Chung MY, Lee HA, Lee SB, Grandillo S, Giovannoni JJ, Lee JM (2023) Natural overexpression of CAROTENOID CLEAVAGE DIOXYGENASE 4 in tomato alters carotenoid flux. Plant Physiol 192:1289–1306
doi: 10.1093/plphys/kiad049 pubmed: 36715630

Auteurs

Chanjeong Jeon (C)

Department of Horticultural Science, College of Agriculture and Life Sciences, Kyungpook National University, Daegu, 41566, Republic of Korea.

Mi-Young Chung (MY)

Department of Agricultural Education, Sunchon National University, Suncheon, 57922, Korea.

Je Min Lee (JM)

Department of Horticultural Science, College of Agriculture and Life Sciences, Kyungpook National University, Daegu, 41566, Republic of Korea. jemin@knu.ac.kr.

Classifications MeSH