Pollen tube growth: critical link in stress tolerance and evolution of angiosperm reproduction?

Ravishankar Palanivelu, School of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA

Sexual reproduction in flowering plants relies on cell-cell interactions such as between the male

gametophyte and the female gametophyte during pollen tube reception, which involves pollen tube

stopping its growth and releasing sperm cells to affect fertilization and seed formation. We

characterized the role of Arabidopsis LORELEI (LRE), a glycosylphosphatidylinositol (GPI)-

anchored membrane protein (GAP), in pollen tube reception and how it functions with its coreceptor

FERONIA in inducing the release of sperm cells for fertilization. Genes encoding these

proteins are members of multi-gene families in most angiosperms and in Arabidopsis, variants of

this signaling complex mediate diverse processes in plant development.

We investigated evolutionary factors underlying the maintenance of gene duplicates in the LRE

gene family. Duplicated genes may acquire new functions (neofunctionalization) and hence may

be retained. Another mechanism of retention is subfunctionalization via sequence variations in the

protein-coding or regulatory regions (regulatory subfunctionalization) of the duplicates. Using

expression analysis and complementation of mutant phenotypes, we showed that

neofunctionalization and regulatory subfunctionalization, but not subfunctionalization, as the

reasons for the retention of LRE-like GAPs (LLG) paralogs in Brassicales.

Interestingly, all but one monocot and all eudicot species examined had an LLG copy with

preferential expression in male reproductive tissues, while the other duplicate copies showed

highest levels of expression in female or vegetative tissues. The single LLG copy in Amborella

trichopoda, a basal angiosperm, is expressed vastly higher in male compared to female reproductive

or vegetative tissues. Because Arabidopsis LLG2 and LLG3, expressed specifically in male

reproductive tissues, are critical for pollen tube growth through the transmitting tract, we propose

that expression of LLGs in male gametophyte underlie the evolutionary innovation of rapid pollen

tube growth in the closed carpel of angiosperms.

Heat stress tolerance is another instance where pollen tube growth is critical for plants, as at

elevated temperatures, pollen tubes fail to grow through the pistil and complete seed formation.

Our central hypothesis is that pollen tubes are uniquely sensitive to heat stress, but that

thermotolerant variants have been selected for reproductive success at high temperature. Using

tomato reproduction as a model system, we are using genomic approaches to define these molecular

adaptations and determine whether they are sufficient to enhance fruit production of

thermosensitive cultivars at high temperature.