Diversification of NOR-like genes resulted in functional similarity in tomato
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Fruit shelf life is an important tomato breeding trait. Ethylene production greatly affects shelf life and is genetically regulated. Tomato ripening is associated with increased ethylene production, and tomato is used as a model for studying fruit ripening, particularly the ethylene biosynthesis and signaling pathways. The key ripening regulator NOR encodes a NAC domain transcription factor which is part of a large plant-specific gene family. Both CRES-T and RNAi gene suppression transgenic lines revealed delayed ripening signs. Further screening of the Micro-Tom ethyl methanesulfonate (EMS)-mutagenized population enabled the selection of alleles responsible for phenotype alterations. Analyses of the transcription levels of ethylene biosynthesis genes ACC synthase (ACS) and ACC-oxidase (ACO) revealed that reduced ethylene production was largely due to transcriptional suppression of ACO1 and ACO3. ACO failed to oxidize the ethylene precursor, thus producing a non-climacteric phenotype in nor. Evidence indicated possible feedback regulation of NOR and cross-regulation of NOR-like genes, and functional conservation suggests that NAC coding genes may undergo functional differentiation. NOR plays a major role in ripening control, whereas NOR-like genes have a minor role; however, a better understanding of NOR-like genes could provide insights into the complex transcriptional regulation of fruit ripening.
KeywordsTranscription factor NAC gene family Subfunctionalization Fruit ripening Tomato
We thank laboratory members at the University of Tsukuba for fruitful discussions on this project. We thank Dr. Nobutaka Mitsuda and Dr. Yoshimi Oshima who provided the CRES-T vectors. This work was supported by JSPS KAKENHI Grant Number 26892006, and Program to Disseminate Tenure Tracking System To N.W., and by JSPS 7 KAKENHI Grant Number 25252008 to H.E. The Micro-Tom seeds were obtained from 8 the National BioResource Project Tomato (NBRP-tomato), supported by AMED, Japan.
NW, MS, TA, MK, and HE designed research; NW, DL, KT, HC, NP and JM performed research; NW, DL, MS, NP, MK and HE analyzed data; and NW, MK and HE wrote the paper.
Compliance with ethical standards
Conflict of interest
The authors declare no conflict of interest.
- Anjanasree KN, Verma PK, Bansal KC (2005) Differential expression of tomato ACC oxidase gene family in relation to fruit ripening. Curr Sci India 89(8):1394–1399Google Scholar
- Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996a) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9(4):525–535. https://doi.org/10.1046/j.1365-313X.1996.09040525.x CrossRefPubMedGoogle Scholar
- Brecht JK (1987) Locular gel formation in developing tomato fruit and the initiation of ethylene production. Hortscience 22(3):476–479Google Scholar
- Du MM, Zhai QZ, Deng L, Li SY, Li HS, Yan LH, Huang Z, Wang B, Jiang HL, Huang TT, Li CB, Wei JN, Kang L, Li JF, Lia CY (2014) Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26(7):3167–3184. https://doi.org/10.1105/tpc.114.128272 CrossRefPubMedPubMedCentralGoogle Scholar
- Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25(2):371–386. https://doi.org/10.1105/tpc.112.108118 CrossRefPubMedPubMedCentralGoogle Scholar
- Giovannoni JJ, Noensie EN, Ruezinsky DM, Lu XH, Tracy SL, Ganal MW, Martin GB, Pillen K, Alpert K, Tanksley SD (1995) Molecular-genetic analysis of the ripening-inhibitor and non-ripening loci of tomato—a first step in genetic map-based cloning of fruit ripening genes. Mol Gen Genet 248(2):195–206. https://doi.org/10.1007/Bf02190801 CrossRefPubMedGoogle Scholar
- Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157(3):1568–1579. https://doi.org/10.1104/pp.111.181107 CrossRefPubMedPubMedCentralGoogle Scholar
- Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
- Nakatsuka A, Shiomi S, Kubo Y, Inaba A (1997) Expression and internal feedback regulation of ACC synthase and ACC oxidase genes in ripening tomato fruit. Plant Cell Physiol 38(10):1103–1110. doi: https://doi.org/10.1093/oxfordjournals.pcp.a029094 CrossRefPubMedGoogle Scholar
- Okabe Y, Asamizu E, Saito T, Matsukura C, Ariizumi T, Bres C, Rothan C, Mizoguchi T, Ezura H (2011) Tomato TILLING technology: development of a reverse genetics tool for the efficient isolation of mutants from Micro-Tom mutant libraries. Plant Cell Physiol 52(11):1994–2005. https://doi.org/10.1093/pcp/pcr134 CrossRefPubMedPubMedCentralGoogle Scholar
- Osorio S, Alba R, Damasceno CMB, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JKC, Fei ZJ, Giovannoni JJ, Fernie AR (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157(1):405–425. https://doi.org/10.1104/pp.111.175463 CrossRefPubMedPubMedCentralGoogle Scholar
- Pereira-Santana A, Alcaraz LD, Castano E, Sanchez-Calderon L, Sanchez-Teyer F, Rodriguez-Zapata L (2015) Comparative genomics of NAC transcriptional factors in angiosperms: implications for the adaptation and diversification of flowering plants. PLoS ONE. https://doi.org/10.1371/journal.pone.0141866 CrossRefPubMedPubMedCentralGoogle Scholar
- Saito T, Ariizumi T, Okabe Y, Asamizu E, Hiwasa-Tanase K, Fukuda N, Mizoguchi T, Yamazaki Y, Aoki K, Ezura H (2011) TOMATOMA: a Novel tomato mutant database distributing Micro-Tom mutant collections. Plant Cell Physiol 52(2):283–296. https://doi.org/10.1093/pcp/pcr004 CrossRefPubMedPubMedCentralGoogle Scholar
- Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:219–241. https://doi.org/10.1146/annurev-arplant-050312-120057 CrossRefPubMedGoogle Scholar
- Wang LL, Hu ZL, Zhu MK, Zhu ZG, Hu JT, Qanmber G, Chen GP (2017) The abiotic stress-responsive NAC transcription factor SlNAC11 is involved in drought and salt response in tomato (Solanum lycopersicum L.). Plant Cell Tiss Org 129(1):161–174. https://doi.org/10.1007/s11240-017-1167-x CrossRefGoogle Scholar
- Yan HD, Zhang AL, Ye YT, Xu B, Chen J, He XY, Wang CR, Zhou SF, Zhang XQ, Peng Y, Ma X, Yan YH, Huang LK (2017) Genome-wide survey of switchgrass NACs family provides new insights into motif and structure arrangements and reveals stress-related and tissue-specific NACs. Sci Rep UK. https://doi.org/10.1038/s41598-017-03435-z CrossRefGoogle Scholar
- Zhu MK, Chen GP, Zhou S, Tu Y, Wang Y, Dong TT, Hu ZL (2014) A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol 55(1):119–135. https://doi.org/10.1093/pcp/pct162 CrossRefPubMedGoogle Scholar