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CLAVATA Signaling Ensures Reproductive Development in Plants across Thermal Environments.

ABSTRACT: The ability to thrive in diverse environments requires that species maintain development and reproduction despite dynamic conditions. Many developmental processes are stabilized through robust signaling pathways that cooperatively ensure proper development.¹ During reproduction, plants like Arabidopsis thaliana continuously generate flowers on growing indeterminate inflorescences.² Flower primordia initiation and outgrowth depends on the hormone auxin and is robust across diverse environments.^3-6 Here, we show that reproductive development under different thermal conditions requires the integration of multiple pathways regulating auxin-dependent flower production. In colder/ambient temperatures, the receptor complex CLAVATA2/CORYNE (CLV2/CRN) is necessary for continuous flower outgrowth during inflorescence development. CLV2/CRN signaling is independent of CLAVATA1 (CLV1)-related receptor signaling but involves the CLAVATA3 INSENSITIVE RECEPTOR KINASE (CIK) family co-receptors, with higher order cik mutant combinations phenocopying clv2/crn flower outgrowth defects. Developing crn inflorescences display reduced auxin signaling, and restoration of auxin biosynthesis is sufficient to restore flower outgrowth in colder and ambient temperatures. In contrast, at higher temperatures, both clv2/crn signaling and heat-induced auxin biosynthesis via YUCCA family genes are synergistically required to maintain flower development. Our work reveals a novel mechanism integrating peptide hormone and auxin signaling in the regulation of flower development across diverse thermal environments.

SUBMITTER: Jones DS

PROVIDER: S-EPMC7855260 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Environments experienced during development have long-lasting consequences for adult performance and fitness. The "environmental matching" hypothesis predicts that individuals perform best when adult and developmental environments match whereas the "silver spoon" hypothesis expects that fitness is higher in individuals developed under favorable environments regardless of adult environments. Temperature and nutrition are the two most influential determinants of environmental quality, but it remains to be elucidated which of these hypotheses better explains the long-term effects of thermal and nutritional histories on adult fitness traits. Here we compared how the temperature and nutrition of larval environment would affect adult survivorship and reproductive success in the fruit fly, Drosophila melanogaster. The aspect of nutrition focused on in this study was the dietary protein-to-carbohydrate (P:C) ratio. The impact of low developmental and adult temperature was to improve adult survivorship. High P:C diet had a negative effect on adult survivorship when ingested during the adult stage, but had a positive effect when ingested during development. No matter whether adult and developmental environments matched or not, females raised in warm and protein-enriched environments produced more eggs than those raised in cool and protein-limiting environments, suggesting the presence of a significant silver spoon effect of larval temperature and nutrition. The effect of larval temperature on adult egg production was weak but persisted across the early adult stage whereas that of larval nutrition was initially strong but diminished rapidly after day 5 posteclosion. Egg production after day 5 was strongly influenced by the P:C ratio of the adult diet, indicating that the diet contributing mainly to reproduction had shifted from larval to adult diet. Our results highlight the importance of thermal and nutritional histories in shaping organismal performance and fitness and also demonstrate how the silver spoon effects of these aspects of environmental histories differ fundamentally in their nature, strength, and persistence.

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CLAVATA Signaling Ensures Reproductive Development in Plants across Thermal Environments.

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