Male gametophyte development in bread wheat (Triticum aestivum L.): molecular, cellular, and biochemical analyses of a sporophytic contribution to pollen wall ontogeny.
Bread wheat (hexaploid AABBDD genome; 16 billion basepairs) is a genetically complex, self-pollinating plant with bisexual flowers that produce short-lived pollen. Very little is known about the molecular biology of its gametophyte development despite a longstanding interest in hybrid seeds. We present here a comprehensive characterization of three apparently homeologous genes (TAA1a, TAA1b and TAA1c) and demonstrate their anther-specific biochemical function. These eight-exon genes, found at only one copy per haploid complement in this large genome, express specifically within the sporophytic tapetum cells. The presence of TAA1 mRNA and protein was evident only at specific stages of pollen development as the microspore wall thickened during the progression of free microspores into vacuolated-microspores. This temporal regulation matched the assembly of wall-impregnated sporopollenin, a phenylpropanoid-lipid polymer containing very long chain fatty alcohols (VLCFAlc), described in the literature. Our results establish that sporophytic genes contribute to the production of fatty alcohols: Transgenic expression of TAA1 afforded production of long/VLCFAlc in tobacco seeds (18 : 1; 20 : 1; 22 : 1; 24 : 0; 26 : 0) and in Escherichia coli (14 : 0; 16 : 0; 18 : 1), suggesting biochemical versatility of TAA1 with respect to cellular milieu and substrate spectrum. Pollen walls additionally contain fatty alcohols in the form of wax esters and other lipids, and some of these lipids are known to play a role in the highly specific sexual interactions at the pollen-pistil interface. This study provides a handle to study these and to manipulate pollen traits, and, furthermore, to understand the molecular biology of fatty alcohol metabolism in general.
Wang
Aiming
A
Plant Biotechnology Institute, National Research Council of Canada, 110 Gymnasium Place, Saskatoon, Saskatchewan, Canada S7N 0W9.
Xia
Qun
Q
Xie
Wenshuang
W
Dumonceaux
Tim
T
Zou
Jitao
J
Datla
Raju
R
Selvaraj
Gopalan
G
D000595:Amino Acid Sequence; D001704:Biopolymers / Q000378:metabolism; D002338:Carotenoids / Q000378:metabolism; D002473:Cell Wall / Q000235:genetics / Q000502:physiology; D018076:DNA, Complementary / Q000737:chemistry / Q000235:genetics; D004926:Escherichia coli / Q000235:genetics; D005227:Fatty Acids / Q000378:metabolism; D005233:Fatty Alcohols / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D017403:In Situ Hybridization; D008969:Molecular Sequence Data; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D030821:Plants, Genetically Modified; D011058:Pollen / Q000737:chemistry / Q000166:cytology / Q000254:growth & development*; D011123:Polyploidy; D012333:RNA, Messenger / Q000378:metabolism; D012098:Reproduction / Q000235:genetics; D012639:Seeds / Q000235:genetics; D017422:Sequence Analysis, DNA; D017386:Sequence Homology, Amino Acid; D014026:Nicotiana / Q000235:genetics; D014908:Triticum / Q000737:chemistry / Q000166:cytology / Q000235:genetics*
D001704:Biopolymers; D018076:DNA, Complementary; D005227:Fatty Acids; D005233:Fatty Alcohols; D010940:Plant Proteins; D012333:RNA, Messenger; C009800:sporopollenin; D002338:Carotenoids