Evidence for the role of transfer cells in the evolutionary increase in seed and fiber biomass yield in cotton

Transfer cells (TCs) are specialized cells exhibiting invaginated wall ingrowths (WIs), thereby amplifying their plasma membrane surface area (PMSA) and hence the capacity to transport nutrients. However, it remains unknown as to whether TCs play a role in biomass yield increase during evolution or domestication. Here, we examine this issue from a comparative evolutionary perspective. The cultivated tetraploid AD genome species of cotton and its A and D genome diploid progenitors displayed high, medium, and low seed and fiber biomass yield, respectively. In all three species, cells of the innermost layer of the seed coat juxtaposed to the filial tissues trans-differentiated to a TC morphology. Electron microscopic analyses revealed that these TCs are characterized by sequential formation of flange and reticulate WIs during the phase of rapid increase in seed biomass. Significantly, TCs from the tetraploid species developed substantially more flange and reticulate WIs and exhibited a higher degree of reticulate WI formation than their progenitors. Consequently, the estimated PMSA of TCs of the tetraploid species was about 4 and 70 times higher than that of TCs of the A and D genome progenitors, respectively, which correlates positively with seed and fiber biomass yield. Further, TCs with extensive WIs in the tetraploid species had much stronger expression of sucrose synthase, a key enzyme involved in TC WI formation and function, than those from the A and D progenitors. The analyses provide a set of novel evidence that the development of TC WIs may play an important role in the increase of seed and fiber biomass yield through polyploidization during evolution.