Lipid Metabolism: Critical Roles in Male Fertility and Other Aspects of Reproductive Development in Plants

Abstract

Fatty acids and their derivatives are essential building blocks for anther cuticle and pollen wall formation. Disruption of lipid metabolism during anther and pollen development often leads to genic male sterility (GMS). To date, many lipid metabolism-related GMS genes that are involved in the formation of anther cuticle, pollen wall, and subcellular organelle membranes in anther wall layers have been identified and characterized. In this review, we summarize recent progress on characterizing lipid metabolism-related genes and their roles in male fertility and other aspects of reproductive development in plants. On the basis of cloned GMS genes controlling biosynthesis and transport of anther cutin, wax, sporopollenin, and tryphine in Arabidopsis, rice, and maize as well as other plant species, updated lipid metabolic networks underlying anther cuticle development and pollen wall formation were proposed. Through bioinformatics analysis of anther RNA-sequencing datasets from three maize inbred lines (Oh43, W23, and B73), a total of 125 novel lipid metabolism-related genes putatively involved in male fertility in maize were deduced. More, we discuss the pathways regulating lipid metabolism-related GMS genes at the transcriptional and post-transcriptional levels. Finally, we highlight recent findings on lipid metabolism-related genes and their roles in other aspects of plant reproductive development. A comprehensive understanding of lipid metabolism, genes involved, and their roles in plant reproductive development will facilitate the application of lipid metabolism-related genes in gene editing, haploid and callus induction, molecular breeding and hybrid seed production in crops.

Normal Structure and Function of Endothecium Chloroplasts Maintained by ZmMs33-Mediated Lipid Biosynthesis in Tapetal Cells Are Critical for Anther Development in Maize

“…In the transcriptome analysis, 12 genes involved in FA de novo biosynthesis, FA unsaturation, and cutin and wax biosynthesis were downregulated in ms33-6038 anthers at stages 8a-9, and 14 genes functioning in FA elongation and degradation were upregulated (Supplemental Figure 6; Supplemental Table 1). Lipid transfer proteins (LTPs) are required for the translocation of lipid components across different anther wall layers to promote formation of the anther cuticle, pollen wall, and subcellular organelle membranes in plant anthers (Wan et al, 2020). Here, we found that most (13/14) of the LTP genes were significantly downregulated in ms33-6038 anthers at stages 7/8a-9 (Supplemental Figure 6).…”

“…Glycerol-3-phosphate acyltransferases (GPATs) catalyze the first step of the glycerolipid synthetic pathway, participate in the biosynthesis of membrane lipids, storage lipids, and extracellular lipid polyesters, and play important roles in anther development and male fertility (Wan et al, 2020). For example, Arabidopsis AtGPAT1 is important for tapetum differentiation and nutrient secretion.…”

“…Anther development requires both independent and cooperative functions of the four anther wall layers because defects in differentiation of one or more somatic layers often lead to male sterility in plants (Walbot and Egger, 2016). Among these layers, the tapetum is the major tissue for synthesis, storage, and transport of various nutrients and structural components for anther cuticle and pollen wall formation, as well as subcellular organelle development (Shi et al, 2015;Li et al, 2017;Wan et al, 2020). For example, most lipid biosynthetic GMS enzymes are localized in the ER and plastids of the tapetum, and most lipid transport proteins are targeted to various membranes and the tapetal cytosol, indicating that lipids are mainly synthesized and transported in the tapetum (Li et al, 2016;Wan et al, 2020).…”

“…Biological studies on genic male sterility (GMS) genes have fundamentally deepened our understanding of plant male reproduction. To date, at least 100 GMS genes have been identified in plants (Yang, 2016;Zhang et al, 2016;Wan et al, , 2020, and at least 17 GMS genes have been reported in maize . For example, Multiple Archesporial Cell 1 (MAC1) , Male Sterile Converted Anther 1 (MSCA1) (Kelliher and Walbot, 2012), Male Sterility 23 (Ms23) (Nan et al, 2017), Ms32 (Moon et al, 2013), and Out Cell Layer 4 (OCL4) (Vernoud et al, 2009) participate in premeiotic morphogenesis, and Abnormal Pollen Vacuolation 1 (APV1) (Somaratne et al, 2017), ZmMs7 (Zhang et al, 2018;An et al, 2020), Irregular Pollen Exine 1 (IPE1)/ZmMs20 (Chen et al, 2017;Wang et al, 2019), Ms26 (Djukanovic et al, 2013), ZmMs30 (An et al, 2019), ZmMs33 (Xie et al, 2018;Zhu et al, 2019), ms44 (Fox et al, 2017), Ms45 (Cigan et al, 2001), and Ms6021 (Tian et al, 2017) are required for anther development and pollen formation during the meiotic and postmeiotic stages in maize.…”

Molecular regulation of ZmMs7 required for maize male fertility and development of a dominant male-sterility system in multiple species

“…The male gamete development is a well-orchestrated process; any disturbance may thus lead to male sterility (9). Up to now, more than 100 GMS genes have been identified in plants (2,10,11), and a great deal of effort has been made to develop biotechnologybased male-sterility systems by using these GMS genes and their…”