Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA.
Proc Natl Acad Sci U S A. 2013 Aug 27;110(35):14480-5. doi: 10.1073/pnas.1305299110. Epub 2013 Aug 12.
During evolution, genomes expanded via whole-genome, segmental, tandem, and individual-gene duplications, and the emerged redundant paralogs would be eliminated or retained owing to selective neutrality or adaptive benefit and further functional divergence. Here we show that tandem paralogs can contribute adaptive quantitative benefit and thus have been retained in a lineage-specific manner. In Brassicaceae, a tandem oleosin gene cluster of five to nine paralogs encodes ample tapetum-specific oleosins located in abundant organelles called tapetosomes in flower anthers. Tapetosomes coordinate the storage of lipids and flavonoids and their transport to the adjacent maturing pollen as the coat to serve various functions. Transfer-DNA and siRNA mutants of Arabidopsis thaliana with knockout and knockdown of different tandem oleosin paralogs had quantitative and correlated loss of organized structures of the tapetosomes, pollen-coat materials, and pollen tolerance to dehydration. Complementation with the knockout paralog restored the losses. Cleomaceae is the family closest to Brassicaceae. Cleome species did not contain the tandem oleosin gene cluster, tapetum oleosin transcripts, tapetosomes, or pollen tolerant to dehydration. Cleome hassleriana transformed with an Arabidopsis oleosin gene for tapetum expression possessed primitive tapetosomes and pollen tolerant to dehydration. We propose that during early evolution of Brassicaceae, a duplicate oleosin gene mutated from expression in seed to the tapetum. The tapetum oleosin generated primitive tapetosomes that organized stored lipids and flavonoids for their effective transfer to the pollen surface for greater pollen vitality. The resulting adaptive benefit led to retention of tandem-duplicated oleosin genes for production of more oleosin and modern tapetosomes.
在进化过程中，基因组通过全基因组、片段、串联和单个基因复制而扩张，出现的冗余旁系同源物会由于选择中性或适应益处而被消除或保留，并进一步发生功能分化。在这里，我们表明串联旁系同源物可以提供适应性的定量益处，因此以谱系特异性的方式被保留下来。在十字花科植物中，有五到九个旁系同源物的串联油体蛋白基因簇编码丰富的位于称为花药绒毡体的大量细胞器中的绒毡层特异性油体蛋白。绒毡体协调脂质和类黄酮的储存及其向相邻成熟花粉的运输作为花粉外壁的涂层，以发挥各种功能。拟南芥的转座子和 siRNA 突变体敲除和敲低不同的串联油体蛋白旁系同源物，导致绒毡体、花粉外壁物质和花粉对脱水的耐受性的有组织结构的定量和相关丧失。敲除旁系同源物的互补恢复了这些损失。藜科是与十字花科最接近的科。藜科植物不含有串联油体蛋白基因簇、绒毡层油体蛋白转录本、绒毡体或对脱水耐受的花粉。拟南芥油体蛋白转化为表达在绒毡层的Cleome hassleriana 具有原始的绒毡体和对脱水耐受的花粉。我们提出，在十字花科植物早期进化过程中，一个油体蛋白基因从种子表达突变到绒毡层。绒毡层油体蛋白产生了原始的绒毡体，这些绒毡体组织储存的脂质和类黄酮，以便有效地将其转移到花粉表面，从而提高花粉活力。由此产生的适应性益处导致串联复制的油体蛋白基因的保留，以产生更多的油体蛋白和现代绒毡体。
