Identification of α-Tomatine 23-Hydroxylase Involved in the Detoxification of a Bitter Glycoalkaloid. (9th December 2019)

• Record Type: Journal Article
• Authors: Nakayasu, Masaru; Akiyama, Ryota; Kobayashi, Midori; Lee, Hyoung Jae; Kawasaki, Takashi; Watanabe, Bunta; Urakawa, Shingo; Kato, Junpei; Sugimoto, Yukihiro; Iijima, Yoko; Saito, Kazuki; Muranaka, Toshiya; Umemoto, Naoyuki; Mizutani, Masaharu
• Is Part Of: Plant & cell physiology. Volume 61:Number 1(2020)
• Page Start: 21
• Page End: 28
• Publication Date: 2019-12-09
• Subjects: 2-Oxoglutarate-dependent dioxygenase -- α-Tomatine -- Fruit ripening -- Sl23DOX -- Steroidal glycoalkaloid -- Tomato (Solanum lycopersicum); Plant physiology -- Periodicals; Microbiology -- Periodicals; Cytology -- Periodicals; Cell Physiology -- Periodicals; Plant Physiological Phenomena -- Periodicals; Cytology; Microbiology; Plant physiology; Periodicals; 571.205
• DOI: 10.1093/pcp/pcz224
• Languages: English
• ISSNs: 0032-0781

Abstract

Abstract: Tomato plants ( Solanum lycopersicum ) contain steroidal glycoalkaloid α-tomatine, which functions as a chemical barrier to pathogens and predators. α-Tomatine accumulates in all tissues and at particularly high levels in leaves and immature green fruits. The compound is toxic and causes a bitter taste, but its presence decreases through metabolic conversion to nontoxic esculeoside A during fruit ripening. This study identifies the gene encoding a 23-hydroxylase of α-tomatine, which is a key to this process. Some 2-oxoglutarate-dependent dioxygenases were selected as candidates for the metabolic enzyme, and Solyc02g062460, designated Sl23DOX, was found to encode α-tomatine 23-hydroxylase. Biochemical analysis of the recombinant Sl23DOX protein demonstrated that it catalyzes the 23-hydroxylation of α-tomatine and the product spontaneously isomerizes to neorickiioside B, which is an intermediate in α-tomatine metabolism that appears during ripening. Leaves of transgenic tomato plants overexpressing Sl23DOX accumulated not only neorickiioside B but also another intermediate, lycoperoside C (23- O -acetylated neorickiioside B). Furthermore, the ripe fruits of Sl23DOX -silenced transgenic tomato plants contained lower levels of esculeoside A but substantially accumulated α-tomatine. Thus, Sl23DOX functions as α-tomatine 23-hydroxylase during the metabolic processing of toxic α-tomatine in tomato fruit ripening and is a key enzyme in the domestication of cultivated tomatoes.