The Reduced Longitudinal Growth Induced by Overexpression of pPLAIIIγ Is Regulated by Genes Encoding Microtubule-Associated Proteins

Abstract

There are three subfamilies of patatin-related phospholipase A (pPLA) group of genes: pPLAI, pPLAII, and pPLAIII. Among the four members of pPLAIIIs (α, β, γ, δ), the overexpression of three isoforms (α, β, and δ) displayed distinct morphological growth patterns, in which the anisotropic cell expansion was disrupted. Here, the least studied pPLAIIIγ was characterized, and it was found that the overexpression of pPLAIIIγ in Arabidopsis resulted in longitudinally reduced cell expansion patterns, which are consistent with the general phenotype induced by pPLAIIIs overexpression. The microtubule-associated protein MAP18 was found to be enriched in a pPLAIIIδ overexpressing line in a previous study. This indicates that factors, such as microtubules and ethylene biosynthesis, are involved in determining the radial cell expansion patterns. Microtubules have long been recognized to possess functional key roles in the processes of plant cells, including cell division, growth, and development, whereas ethylene treatment was reported to induce the reorientation of microtubules. Thus, the possible links between the altered anisotropic cell expansion and microtubules were studied. Our analysis revealed changes in the transcriptional levels of microtubule-associated genes, as well as phospholipase D (PLD) genes, upon the overexpression of pPLAIIIγ. Overall, our results suggest that the longitudinally reduced cell expansion observed in pPLAIIIγ overexpression is driven by microtubules via transcriptional modulation of the PLD and MAP genes. The altered transcripts of the genes involved in ethylene-biosynthesis in pPLAIIIγOE further support the conclusion that the typical phenotype is derived from the link with microtubules.

A group III patatin-like phospholipase gene pPLAIIIδ regulates lignin biosynthesis and influences the rate of seed germination in Arabidopsis thaliana

“…The root hair length was not significantly changed in pPLAIIIδ:RNAi lines, but root hair density increased in pPLAIIIδ:RNAi #11 ( Figures 2H–J ). The observed phenotypic results support previously reported effect of pPLAIII genes OE in impeding anisotropic cell expansion ( Li et al., 2011 ; Jang and Lee, 2020a ; Jang and Lee, 2020b ; Jang et al., 2020 ; Jang et al., 2021 ; Jang et al., 2022 ). The decreased size of pPLAIIIδ-OE plants coincided with the downregulation of genes regulating active gibberellic acid (GA) biosynthesis, GA20ox1 and GA3ox1 ( Supplementary Figure 2B ).…”

“…Overall, depending on the threshold level of the mRNA expression of pPLAIIIs , overexpression drives reduced longitudinal growth, while silencing promotes overall growth. The pPLAIIIs -influcenced growth alterations have been linked to several internal processes such as changes in macrotubule-associated proteins ( Jang et al., 2021 ), and altered GA metabolism ( Liu et al., 2015 ). This study has shown that decreased transcript level of GA biosynthesis genes could be another underlying mechanism for dwarf phenotype seen in OE lines.…”

“…Apart from hydrolyzing phospho/galactolipids, pPLAIII enzymes (pPLAIIIα, β, γ, and δ) are also involved in plant responses to abiotic stress, auxin signaling ( Scherer et al., 2010 ), and in resistance to viral diseases ( Jang et al., 2020 ). Also, pPLAIIIs influence the development of vegetative tissues and seeds ( Li et al., 2011 ; Liu et al., 2015 ; Jang et al., 2021 ). Previous studies have indicated that pPLAIIIδ is specifically involved in several cellular functions, including growth, organ development, and signal transduction ( Li et al., 2013 ; Dong et al., 2014 ; Li et al., 2015 ).…”

Overexpression of pPLAIIIγ in Arabidopsis Reduced Xylem Lignification of Stem by Regulating Peroxidases

“…Two selected transgenic pPLAIIIγOE lines displayed intermediate and severely dwarfed plant height (Figure 2B). Isotropic growth patterns [15] were more distinctively observed in the stem (Figure 2C), which ultimately led to shorter plant height in OE lines than that in the Col-0 lines. A-E,G,H) and 1 cm (F).…”

“…All the overexpression lines of pPLAIIIαOE [5,11], pPLAIIIβOE [3,4,10], and pPLAIIIδOE [14] displayed overall stunted growth patterns with reduced plant height and radially expanded cell elongation. Reduced longitudinal growth patterns, in which the anisotropic cell expansion was disrupted, focused on floral organs and leaves and were very recently published by overexpression of pPLAIIIγ (pPLAIIIγOE) [15]. However, the phenotypic and biochemical characteristics of pPLAIIIγOE in stem elongation and lignification were not yet characterized.…”