Semi-dominant effects of a novel ripening inhibitor (rin) locus allele on tomato fruit ripening.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101285081 Publication Model: eCollection Cited Medium: Internet ISSN: 1932-6203 (Electronic) Linking ISSN: 19326203 NLM ISO Abbreviation: PLoS One Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science

Genes, Dominant* ; Mutation*; Ethylenes/*metabolism ; Fruit/*growth & development ; Solanum lycopersicum/*growth & development ; MADS Domain Proteins/*metabolism ; Plant Proteins/*metabolism; Fruit/genetics ; Fruit/metabolism ; Gene Expression Regulation, Plant ; Solanum lycopersicum/genetics ; Solanum lycopersicum/metabolism ; MADS Domain Proteins/genetics ; Phenotype ; Plant Proteins/genetics

The tomato (Solanum lycopersicum) ripening inhibitor (rin) mutation completely represses fruit ripening, as rin fruits fail to express ripening-associated genes and remain green and firm. Moreover, heterozygous rin fruits (rin/+) ripen normally but have extended shelf life, an important consideration for this perishable fruit crop; therefore, heterozygous rin has been widely used to breed varieties that produce red tomatoes with improved shelf life. We previously used CRISPR/Cas9 to produce novel alleles at the rin locus. The wild-type allele RIN encodes a MADS-box transcription factor and the novel allele, named as rinG2, generates an early stop codon, resulting in C-terminal truncation of the transcription factor. Like rin fruits, rinG2 fruits exhibit extended shelf life, but unlike rin fruits, which remain yellow-green even after long-term storage, rinG2 fruits turn orange due to ripening-associated carotenoid production. Here, to explore the potential of the rinG2 mutation for breeding, we characterized the effects of rinG2 in the heterozygous state (rinG2/+) compared to the effects of rin/+. The softening of rinG2/+ fruits was delayed compared to the wild type but to a lesser degree than rin/+ fruits. Lycopene and β-carotene levels in rinG2/+ fruits were similar to those of the wild type, whereas rin/+ fruits accumulated half the amount of β-carotene compared to the wild type. The rinG2/+ fruits produced lower levels of ethylene than wild-type and rin/+ fruits. Expression analysis revealed that in rinG2/+ fruits, the rinG2 mutation (like rin) partially inhibited the expression of ripening-associated genes. The small differences in the inhibitory effects of rinG2 vs. rin coincided with small differences in phenotypes, such as ethylene production, softening, and carotenoid accumulation. Therefore, rinG2 represents a promising genetic resource for developing tomato cultivars with extended shelf life.
Competing Interests: The authors have declared that no competing interests exist.

Plant Sci. 2020 May;294:110436. (PMID: 32234221)
Science. 2002 Apr 12;296(5566):343-6. (PMID: 11951045)
Proc Natl Acad Sci U S A. 2010 Feb 9;107(6):2413-8. (PMID: 20133661)
Plant J. 2010 Oct;64(1):140-50. (PMID: 20659278)
Plant Mol Biol. 2013 Jul;82(4-5):427-38. (PMID: 23677393)
J Exp Bot. 2014 Jul;65(12):3005-14. (PMID: 24723399)
Plant Physiol. 1998 Mar;116(3):1145-50. (PMID: 9501147)
Plant Cell. 2014 Jan;26(1):89-101. (PMID: 24415769)
Plant Physiol. 1994 Oct;106(2):429-436. (PMID: 12232340)
Plant Cell. 2007 Oct;19(10):3194-211. (PMID: 17933904)
FEBS J. 2008 Feb;275(3):527-35. (PMID: 18167141)
Trends Plant Sci. 2018 Apr;23(4):302-310. (PMID: 29429585)
Plant Cell. 2012 Nov;24(11):4437-51. (PMID: 23136376)
Plant Biotechnol J. 2020 Jan;18(1):106-118. (PMID: 31131540)
Nat Plants. 2017 Nov;3(11):866-874. (PMID: 29085071)
Plant Cell. 2013 Feb;25(2):371-86. (PMID: 23386264)
Genet Mol Res. 2003 Sep 30;2(3):317-27. (PMID: 14966680)
Plant Physiol. 2012 Jan;158(1):439-50. (PMID: 22106095)
J Biol Chem. 2001 Jul 27;276(30):28051-7. (PMID: 11375393)
Plant Physiol. 1999 Jun;120(2):383-90. (PMID: 10364389)
Biochem Biophys Res Commun. 2015 Nov 6;467(1):76-82. (PMID: 26408904)
New Phytol. 2020 Apr;226(2):460-475. (PMID: 31814125)
Plant Physiol. 2002 Aug;129(4):1755-62. (PMID: 12177488)
Plant Physiol. 2007 Aug;144(4):1960-7. (PMID: 17556513)
Plant J. 2012 Apr;70(2):243-55. (PMID: 22098335)
Plant Physiol. 1998 Dec;118(4):1295-305. (PMID: 9847103)
BMC Plant Biol. 2008 Dec 22;8:131. (PMID: 19102748)
Plant Cell. 2004;16 Suppl:S170-80. (PMID: 15010516)
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11102-7. (PMID: 10995464)
Planta. 2012 Jun;235(6):1107-22. (PMID: 22160566)
Curr Opin Plant Biol. 2007 Jun;10(3):283-9. (PMID: 17442612)
Plant Biotechnol J. 2017 Dec;15(12):1544-1555. (PMID: 28371176)
Plant Physiol. 2000 Jul;123(3):979-86. (PMID: 10889246)
Plant J. 2008 Jul;55(2):212-23. (PMID: 18363783)
Nat Biotechnol. 2013 Feb;31(2):154-9. (PMID: 23354102)
Plant Physiol. 2007 Jun;144(2):1012-28. (PMID: 17449643)
Plant Physiol. 2020 May;183(1):80-95. (PMID: 32094307)
Plant Physiol. 2018 Jan;176(1):891-909. (PMID: 29133374)
Biosci Biotechnol Biochem. 2014;78(2):231-7. (PMID: 25036675)
New Phytol. 2019 Mar;221(4):1724-1741. (PMID: 30328615)
Methods. 2001 Dec;25(4):402-8. (PMID: 11846609)
Plant Physiol. 2011 Nov;157(3):1568-79. (PMID: 21941001)
Proc Natl Acad Sci U S A. 1988 Dec;85(23):8805-9. (PMID: 16593997)
Plant Mol Biol. 1990 Mar;14(3):369-79. (PMID: 2102820)
Nat Genet. 2006 Aug;38(8):948-52. (PMID: 16832354)
Plant Cell. 1989 Jan;1(1):53-63. (PMID: 2535467)
Plant Cell. 1999 Nov;11(11):2203-16. (PMID: 10559444)
Nat Biotechnol. 2016 Sep;34(9):950-2. (PMID: 27454737)

0 (Ethylenes)
0 (MADS Domain Proteins)
0 (Plant Proteins)

Date Created: 20210422 Date Completed: 20210917 Latest Revision: 20221207

20221213

PMC8061929

10.1371/journal.pone.0249575

33886595