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Increased ACS Enzyme Dosage Causes Initiation of Climacteric Ethylene Production in Tomato.
Int J Mol Sci. 2022 Sep 15; 23(18)IJ

Abstract

Fruits of wild tomato species show different ethylene-dependent ripening characteristics, such as variations in fruit color and whether they exhibit a climacteric or nonclimacteric ripening transition. 1-Aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO) are key enzymes in the ethylene biosynthetic pathway encoded by multigene families. Gene duplication is a primary driver of plant diversification and angiosperm evolution. Here, interspecific variations in the molecular regulation of ethylene biosynthesis and perception during fruit ripening in domesticated and wild tomatoes were investigated. Results showed that the activated ACS genes were increased in number in red-ripe tomato fruits than in green-ripe tomato fruits; therefore, elevated dosage of ACS enzyme promoted ripening ethylene production. Results showed that the expression of three ACS isogenes ACS1A, ACS2, and ACS4, which are involved in autocatalytic ethylene production, was higher in red-ripe tomato fruits than in green-ripe tomato fruits. Elevated ACS enzyme dosage promoted ethylene production, which corresponded to the climacteric response of red-ripe tomato fruits. The data suggest that autoinhibitory ethylene production is common to all tomato species, while autocatalytic ethylene production is specific to red-ripe species. The essential regulators Non-ripening (NOR) and Ripening-Inhibitor (RIN) have experienced gene activation and overlapped with increasing ACS enzyme dosage. These complex levels of transcript regulation link higher ethylene production with spatiotemporal modulation of gene expression in red-ripe tomato species. Taken together, this study shows that bursts in ethylene production that accompany fruit color changes in red-ripe tomatoes are likely to be an evolutionary adaptation for seed dispersal.

Authors+Show Affiliations

Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan.Department of Horticulture, Zhejiang University, Hangzhou 310058, China.Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan. RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Kanagawa, Japan. Tsukuba Plant Innovation Research Center, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan.Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan. Tsukuba Plant Innovation Research Center, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan.Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan. Tsukuba Plant Innovation Research Center, University of Tsukuba, Tsukuba 305-8572, Ibaraki, Japan.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

36142701

Citation

Chen, Haoting, et al. "Increased ACS Enzyme Dosage Causes Initiation of Climacteric Ethylene Production in Tomato." International Journal of Molecular Sciences, vol. 23, no. 18, 2022.
Chen H, Bai S, Kusano M, et al. Increased ACS Enzyme Dosage Causes Initiation of Climacteric Ethylene Production in Tomato. Int J Mol Sci. 2022;23(18).
Chen, H., Bai, S., Kusano, M., Ezura, H., & Wang, N. (2022). Increased ACS Enzyme Dosage Causes Initiation of Climacteric Ethylene Production in Tomato. International Journal of Molecular Sciences, 23(18). https://doi.org/10.3390/ijms231810788
Chen H, et al. Increased ACS Enzyme Dosage Causes Initiation of Climacteric Ethylene Production in Tomato. Int J Mol Sci. 2022 Sep 15;23(18) PubMed PMID: 36142701.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Increased ACS Enzyme Dosage Causes Initiation of Climacteric Ethylene Production in Tomato. AU - Chen,Haoting, AU - Bai,Songling, AU - Kusano,Miyako, AU - Ezura,Hiroshi, AU - Wang,Ning, Y1 - 2022/09/15/ PY - 2022/08/15/received PY - 2022/09/06/revised PY - 2022/09/12/accepted PY - 2022/9/23/entrez PY - 2022/9/24/pubmed PY - 2022/9/28/medline KW - climacteric KW - ethylene biosynthesis KW - fruit ripening KW - gene duplication KW - wild tomato JF - International journal of molecular sciences JO - Int J Mol Sci VL - 23 IS - 18 N2 - Fruits of wild tomato species show different ethylene-dependent ripening characteristics, such as variations in fruit color and whether they exhibit a climacteric or nonclimacteric ripening transition. 1-Aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO) are key enzymes in the ethylene biosynthetic pathway encoded by multigene families. Gene duplication is a primary driver of plant diversification and angiosperm evolution. Here, interspecific variations in the molecular regulation of ethylene biosynthesis and perception during fruit ripening in domesticated and wild tomatoes were investigated. Results showed that the activated ACS genes were increased in number in red-ripe tomato fruits than in green-ripe tomato fruits; therefore, elevated dosage of ACS enzyme promoted ripening ethylene production. Results showed that the expression of three ACS isogenes ACS1A, ACS2, and ACS4, which are involved in autocatalytic ethylene production, was higher in red-ripe tomato fruits than in green-ripe tomato fruits. Elevated ACS enzyme dosage promoted ethylene production, which corresponded to the climacteric response of red-ripe tomato fruits. The data suggest that autoinhibitory ethylene production is common to all tomato species, while autocatalytic ethylene production is specific to red-ripe species. The essential regulators Non-ripening (NOR) and Ripening-Inhibitor (RIN) have experienced gene activation and overlapped with increasing ACS enzyme dosage. These complex levels of transcript regulation link higher ethylene production with spatiotemporal modulation of gene expression in red-ripe tomato species. Taken together, this study shows that bursts in ethylene production that accompany fruit color changes in red-ripe tomatoes are likely to be an evolutionary adaptation for seed dispersal. SN - 1422-0067 UR - https://www.unboundmedicine.com/medline/citation/36142701/Increased_ACS_Enzyme_Dosage_Causes_Initiation_of_Climacteric_Ethylene_Production_in_Tomato_ DB - PRIME DP - Unbound Medicine ER -