Fatty acid amide hydrolase and 9-lipoxygenase modulate cotton seedling growth by ethanolamide oxylipin levels

Abstract

Polyunsaturated N-acylethanolamines (NAEs) can be hydrolyzed by fatty acid amide hydrolase (FAAH) or oxidized by lipoxygenase (LOX). In Arabidopsis (Arabidopsis thaliana), the 9-LOX product of linoleoylethanolamide, namely, 9-hydroxy linoleoylethanolamide (9-NAE-HOD), is reported to negatively regulate seedling development during secondary dormancy. In upland cotton (Gossypium hirsutum L.), six putative FAAH genes (from two diverged groups) and six potential 9-LOX genes are present; however, their involvement in 9-NAE-HOD metabolism and its regulation of seedling development remain unexplored. Here, we report that in cotton plants, two specific FAAH isoforms (GhFAAH Ib and GhFAAH IIb) are needed for hydrolysis of certain endogenous NAEs. Virus-induced gene silencing (VIGS) of either or both FAAHs led to reduced seedling growth and this coincided with reduced amidohydrolase activities and elevated quantities of endogenous 9-NAE-HOD. Transcripts of GhLOX21 were consistently elevated in FAAH-silenced tissues, and co-silencing of GhLOX21 and GhFAAH (Ib and/or IIb) led to reversal of seedling growth to normal levels (comparable to no silencing). This was concomitant with reductions in the levels of 9-NAE-HOD, but not of 13-NAE-HOD. Pharmacological experiments corroborated the genetic and biochemical evidence, demonstrating that direct application of 9-NAE-HOD, but not 13-NAE-HOD or their corresponding free fatty acid oxylipins, inhibited the growth of cotton seedlings. Additionally, VIGS of GhLOX21 in cotton lines overexpressing AtFAAH exhibited enhanced growth and no detectable 9-NAE-HOD. Altogether, we conclude that growth of cotton seedlings involves fine-tuning of 9-NAE-HOD levels via FAAH-mediated hydrolysis and LOX-mediated production, expanding the mechanistic understanding of plant growth modulation by NAE oxylipins to a perennial crop species.

Growth, leaf anatomy, and photosynthesis of cotton (Gossypium hirsutum L.) seedlings in response to four light-emitting diodes and high pressure sodium lamp

“…For instance, our previous study (Wang et al, 2012) was carried out in a growth chamber to elucidate the phytohormone basis of the feedback regulation of leaf senescence induced by potassium deficiency in cotton. The study conducted by Arias-Gaguancela et al (2023) in a controlled environment revealed the mechanistic understanding of cotton growth modulation by NAE (9-hydroxy linoleoylethanolamide) oxylipins. As mentioned above, there is also a tendency for LEDs to replace HSP lamps in cotton-grown chambers.…”

Genetic and Morpho-Physiological Differences among Transgenic and No-Transgenic Cotton Cultivars

“…Overexpression of Spinacia oleracea KASIII (SoKASIII) in tobacco leaves under the control of the 35S CaMV promoter and of Jatropha Curcas KASIII (ChKASIII) in A. thaliana and oilseed rape seeds under the control of the napin promoter, indicates that the 16:0 fatty acid contents of both transgenic plants were significantly increased [42]. In recent years, efforts have been made to manipulate key fatty acid synthetic genes in various species using transgenic technology [43][44][45][46][47]. Transformations using transgenes encoding key enzymes or enzyme subunits have resulted in the alteration in lipid levels to varying degrees [37,48], and in some cases, the oil content was reduced [49].…”

Osmotic stress in roots drives lipoxygenase-dependent plastid remodeling through singlet oxygen production

“…Lipoxygenase type 13 is recognized for its role in jasmonic acid (JA) production (Maynard et al, 2021; Xing et al, 2019). Lipoxygenase type 9 produce other stress responses (Vellosillo et al 2013; (Arias-Gaguancela et al, 2023; Jimenez-Aleman and Jander, 2023; Vellosillo et al, 2007).…”