Deregulation of ¿-carotene desaturase in Arabidopsis and tomato exposes a unique carotenoid-derived redundant regulation of floral meristem identity and function

Authors: MCQUINN, RYAN - Australian National University; LEROUX, JULIE - Australian National University; SIERRA, JULIO - Universidad Nacianal Autonoma De Mexico; ESCOBAR-TOVAR, LINA - Universidad Nacianal Autonoma De Mexico; FRUSCIANTE, SARA - Enea Casaccia Research Center; FINNEGAN, E. JEAN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); DIRETTI, GIANFRANCO - Enea Casaccia Research Center; GIULIANO, GIOVANNI - Enea Casaccia Research Center; Giovannoni, James; LEON, PATRICIA - Universidad Nacianal Autonoma De Mexico; POGSON, BARRY - Australian National University

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/26/2023
Publication Date: 3/2/2023
Citation: Mcquinn, R., Leroux, J., Sierra, J., Escobar-Tovar, L., Frusciante, S., Finnegan, E., Diretti, G., Giuliano, G., Giovannoni, J.J., Leon, P., Pogson, B. 2023. Deregulation of ¿-carotene desaturase in Arabidopsis and tomato exposes a unique carotenoid-derived redundant regulation of floral meristem identity and function. The Plant Journal. 114(4):783-804. https://doi.org/10.1111/tpj.16168.
DOI: https://doi.org/10.1111/tpj.16168

Interpretive Summary: Establishing and maintaining floral meristem (FM) identity is paramount for plant reproductive success underpinning the production of fruits and grains that contribute to food security. Events leading to the emergence of the FM involve an elaborate reprogramming of gene regulatory networks in response to environmental factors (e.g. day length, abiotic stress) and endogenous cues, thereby driving the transition from a vegetative to a reproductive state. The timing of flowering with respect to season, environment and development is critical to the reproductive success of most plant species. Here we demonstrate that ZDS, a gene involved in carotenoid pigment synthesis, is uniquely regulated during early stages of flower development when FM identity is established under indirect control of the FM identity master regulator gene AP1. We show that removal of the '-carotene-derived apocarotenoid signal resulting from ZDS activity through the constitutive over-expression of ZDS, impairs floral meristem termination in tomato and supporting the role of this gene in the floral transition necessary for fruit formation.

Technical Abstract: A level of redundancy and interplay among the transcriptional regulators of floral development safeguards a plant's reproductive success and ensures crop production. In the present study, an additional layer of complexity in the regulation of floral meristem (FM) identity and flower development is elucidated linking carotenoid biosynthesis and metabolism to the regulation of determinate flowering. The accumulation and subsequent cleavage of a diverse array of '-carotenes in the chloroplast biogenesis 5 (clb5) mutant of Arabidopsis results in the reprogramming of meristematic gene regulatory networks establishing FM identity mirroring that of the FM identity master regulator, APETALA1 (AP1). The immediate transition to floral development in clb5 requires long photoperiods in a GIGANTEA-independent manner, whereas AP1 is essential for the floral organ development of clb5. The elucidation of this link between carotenoid metabolism and floral development translates to tomato exposing a regulation of FM identity redundant to and initiated by AP1 and proposed to be dependent on the E class floral initiation and organ identity regulator, SEPALLATA3 (SEP3).