flasher, a novel mutation in a glucosinolate modifying enzyme, conditions changes in plant architecture and hormone homeostasis

• Published in: The Plant journal : for cell and molecular biology Vol. 103; no. 6; pp. 1989 - 2006
• Main Authors: Garrido, Ameth N., Supijono, Esther, Boshara, Peter, Douglas, Scott J., Stronghill, Patti E., Li, Baohua, Nambara, Eiji, Kliebenstein, Daniel J., Riggs, C. Daniel
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.09.2020
• Subjects: Arabidopsis - anatomy & histology; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis Proteins - physiology; Architecture; Biosynthesis; Cloning; Complementation; cytokinin; Cytokinins; development; Elongation; Enzymes; Fecundity; Feedback control; Flavin; Flowering; Flowers - anatomy & histology; Flowers - genetics; Follicle-stimulating hormone; Gene expression; Genes; Gibberellins; glucosinolate; Glucosinolates - metabolism; Homeodomain Proteins - genetics; Homeodomain Proteins - metabolism; Homeodomain Proteins - physiology; Homeostasis; Homeostasis - genetics; jasmonate; Jasmonic acid; KNOX gene; meristem; Meristems; Metabolites; Monooxygenase; Mutation; Mutation - genetics; Plant Growth Regulators - metabolism; Plant Growth Regulators - physiology; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Proteins - physiology; Senescence; small molecule effector; Substrates; Suppressor mutant; Vascular system (plant anatomy); development; glucosinolate; cytokinin; meristem; jasmonate; small molecule effector; KNOX gene
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14878

SUMMARY Meristem function is underpinned by numerous genes that affect hormone levels, ultimately controlling phyllotaxy, the transition to flowering and general growth properties. Class I KNOX genes are major contributors to this process, promoting cytokinin biosynthesis but repressing gibberellin production to condition a replication competent state. We identified a suppressor mutant of the KNOX1 mutant brevipedicellus (bp) that we termed flasher (fsh), which promotes stem and pedicel elongation, suppresses early senescence, and negatively affects reproductive development. Map‐based cloning and complementation tests revealed that fsh is due to an E40K change in the flavin monooxygenase GS‐OX5, a gene encoding a glucosinolate (GSL) modifying enzyme. In vitro enzymatic assays revealed that fsh poorly converts substrate to product, yet the levels of several GSLs are higher in the suppressor line, implicating FSH in feedback control of GSL flux. FSH is expressed predominantly in the vasculature in patterns that do not significantly overlap those of BP, implying a non‐cell autonomous mode of meristem control via one or more GSL metabolites. Hormone analyses revealed that cytokinin levels are low in bp, but fsh restores cytokinin levels to near normal by activating cytokinin biosynthesis genes. In addition, jasmonate levels in the fsh suppressor are significantly lower than in bp, which is likely due to elevated expression of JA inactivating genes. These observations suggest the involvement of the GSL pathway in generating one or more negative effectors of growth that influence inflorescence architecture and fecundity by altering the balance of hormonal regulators. Significance Statement Glucosinolates are secondary metabolites produced primarily by plants of the order Brassicales, and they and/or their catabolites are known to play roles in plant defense, flowering time, drought tolerance, growth and development. Here we report that a mutation in a glucosinolate modifying enzyme influences KNOX1‐mediated development, in part by influencing the levels of cytokinin and the jasmonate JA‐Ile.