An evolutionary view of vanillylamine synthase pAMT, a key enzyme of capsaicinoid biosynthesis pathway in chili pepper.

Autor: Kusaka, Hirokazu, Nakasato, Saika, Sano, Kaori, Kobata, Kenji, Ohno, Sho, Doi, Motoaki, Tanaka, Yoshiyuki
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Zdroj: Plant Journal; Mar2024, Vol. 117 Issue 5, p1453-1465, 13p
Abstrakt: SUMMARY: Pungent capsaicinoid is synthesized only in chili pepper (Capsicum spp.). The production of vanillylamine from vanillin is a unique reaction in the capsaicinoid biosynthesis pathway. Although putative aminotransferase (pAMT) has been isolated as the vanillylamine synthase gene, it is unclear how Capsicum acquired pAMT. Here, we present a phylogenetic overview of pAMT and its homologs. The Capsicum genome contained 5 homologs, including pAMT, CaGABA‐T1, CaGABA‐T3, and two pseudogenes. Phylogenetic analysis indicated that pAMT is a member of the Solanaceae cytoplasmic GABA‐Ts. Comparative genome analysis found that multiple copies of GABA‐T exist in a specific Solanaceae genomic region, and the cytoplasmic GABA‐Ts other than pAMT are located in the region. The cytoplasmic GABA‐T was phylogenetically close to pseudo‐GABA‐T harboring a plastid transit peptide (pseudo‐GABA‐T3). This suggested that Solanaceae cytoplasmic GABA‐Ts occurred via duplication of a chloroplastic GABA‐T ancestor and subsequent loss of the plastid transit signal. The cytoplasmic GABA‐T may have been translocated from the specific Solanaceae genomic region during Capsicum divergence, resulting in the current pAMT locus. A recombinant protein assay demonstrated that pAMT had higher vanillylamine synthase activity than those of other plant GABA‐Ts. pAMT was expressed exclusively in the placental septum of mature green fruit, whereas tomato orthologs SlGABA‐T2/4 exhibit a ubiquitous expression pattern in plants. These findings suggested that both the increased catalytic efficiency and transcriptional changes in pAMT may have contributed to establish vanillylamine synthesis in the capsaicinoid biosynthesis pathway. This study provides insights into the establishment of pungency in the evolution of chili peppers. Significance Statement: Chili pepper vanillylamine synthase (pAMT) in capsaicin biosynthesis pathway belongs to the Solanaceae cytoplasmic GABA‐Ts, which originated via duplication of a chloroplastic ancestor and exhibits higher catalytic efficiency and placenta‐specific expression, compared with other close‐related GABA‐Ts. This study presents an intriguing case of how a primary metabolism enzyme evolved into a key enzyme that contributes to lineage‐specific secondary metabolite biosynthesis. [ABSTRACT FROM AUTHOR]
Databáze: Complementary Index