Mutation of ACX1, a Jasmonic Acid Biosynthetic Enzyme, Leads to Petal Degeneration in Chinese Cabbage (Brassica campestris ssp. pekinensis).

Shenling Peng,Hui Feng,Shengnan Huang,Zhiyong Liu

doi:10.3390/ijms20092310

Shenling Peng, Hui Feng + Show 2 more

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https://doi.org/10.3390/ijms20092310

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Abstract

Petal color, size, and morphology play important roles in protecting other floral organs, attracting pollinators, and facilitating sexual reproduction in plants. In a previous study, we obtained a petal degeneration mutant (pdm) from the ‘FT’ doubled haploid line of Chinese cabbage and found that the candidate gene for pdm, Bra040093, encodes the enzyme acyl-CoA oxidase1. In this study, we sought to examine the gene networks regulating petal development in pdm plants. We show that the mRNA and protein expression of Bra040093, which is involved in the jasmonic acid (JA) biosynthetic pathway, were significantly lower in the petals of pdm plants than in those of ‘FT’ plants. Similarly, the JA and methyl jasmonate (MeJA) contents of petals were significantly lower in pdm plants than in ‘FT’ plants and we found that exogenous application of these hormones to the inflorescences of pdm plants restored the ‘FT’ phenotype. Comparative analyses of the transcriptomes of ‘FT’, pdm and pdm + JA (pJA) plants revealed 10,160 differentially expressed genes (DEGs) with consistent expression tendencies in ‘FT’ vs. pdm and pJA vs. pdm comparisons. Among these DEGs, we identified 69 DEGs related to floral organ development, 11 of which are involved in petal development regulated by JA. On the basis of qRT-PCR verification, we propose regulatory pathways whereby JA may mediate petal development in the pdm mutant. We demonstrate that mutation of Bra040093 in pdm plants leads to reduced JA levels and that this in turn promotes changes in the expression of genes that are expressed in response to JA, ultimately resulting in petal degeneration. These findings thus indicate that JA is associated with petal development in Chinese cabbage. These results enhance our knowledge on the molecular mechanisms underlying petal development and lay the foundations for further elucidation of the mechanisms associated with floral organ development in Chinese cabbage.

Highlights

IntroductionFloral organs play essential roles in sexual reproduction [1,2]. The morphological development of floral organs is a highly complex and inherently stable process that is an indispensable facet of plant growth and development
In plants, floral organs play essential roles in sexual reproduction [1,2]
Compared with the ‘FLOWERING LOCUS T (FT)’ wild-type Chinese cabbage, we found that Bra040093 is down-regulated in pdm mutant plants and, hypothesize that the Bra040093 mutation in pdm might hinder jasmonic acid (JA) biosynthesis and affect petal development

Summary

Introduction

Floral organs play essential roles in sexual reproduction [1,2]. The morphological development of floral organs is a highly complex and inherently stable process that is an indispensable facet of plant growth and development. The process is regulated by the expression of multiple genes and Coen and Meyerowitz [3] have identified many functional genes related to the regulation of floral organ development in homeotic mutants of model plants, including Arabidopsis thaliana and Antirrhinum majus, on the basis of which they proposed the ABC model of floral organ development. In Arabidopsis thaliana, AINTEGUMENTA (ANT) encodes an AP2-domain family transcription factor that acts downstream of AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE (ARGOS), and overexpression of ANT results in increases in the size of leaves, inflorescences, and floral organs [8]. Studies on the double mutant bpe-arf have shown that, at the early stage of petal development, BPEp and Auxin response factors (ARF8) synergistically limit mitotic cell growth, whereas at the late stage of petal development, the proteins encoded by these genes interact to limit cell expansion, thereby regulating petal size [15,16]

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