PerspectivePlant Science

Reproductive Dialog

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Science  03 Aug 2007:
Vol. 317, Issue 5838, pp. 606-607
DOI: 10.1126/science.1146655

Fertilization in higher plants requires intricate signaling between the male and female. The molecular details underlying this communication are of great interest, not only to understand plant reproduction but also to guide efforts in crossing plant species to generate new hybrids. On page 656 of this issue, Escobar-Restrepo et al. (1) show that cells in the female ovule express a protein—a type of receptor that is widely known to mediate cell-cell communication—that is required for fertilization. The unknown ligand(s) for the receptor may be present on or secreted by the pollen tube. Such a receptor-ligand interaction could control species-specific reproduction.

In flowering plants, the pollen grain (male gametophyte) contains three cells: a vegetative cell that will form the pollen tube, and two sperm cells. After release from the anther and landing on the stigma, the pollen grain extends a tube through the style, toward the ovule (see the figure). Within each ovule, there is an embryo sac (female gametophyte), typically composed of seven cells: an egg cell, a central cell, two synergid cells, and three antipodal cells. The pollen tube enters the ovule through an opening (the micropyle), penetrates one of the synergids, and bursts, thereby releasing the sperm cells. One sperm cell fuses with the egg cell to form a zygote, while the other sperm cell fuses with the central cell to form the primary endosperm cell.

Fertilization communication.

Synergid cells that attract pollen tubes express FERONIA protein. A ligand from the pollen tube may interact with FERONIA, causing the pollen tube to stop growing and release sperm cells.

CREDIT: P. HUEY/SCIENCE

A few years ago, two female gametophytic mutants, feronia (2) and sirène (3), were described in the flowering plant Arabidopsis thaliana. In these mutant plants, pollen tubes were attracted to ovules and entered the micropyle, but failed to burst and release sperm, continuing to grow instead. This phenotype suggested failed communication between the pollen tube and the embryo sac, but it was not known whether feronia and sirène affected the same or different components in this dialog. Escobar-Restrepo et al. now show that both mutants have lesions in the same gene and that the gene encodes an enzyme that phosphorylates proteins on serine and threonine residues. The enzyme, FERONIA, belongs to the previously uncharacterized CrRLK1L-1 group of receptor-like kinases (4), of which there are 15 members in A. thaliana. The authors determined that FERONIA is located in the plasma membrane of the synergid cells.

Because the pollen tube overgrowth phenotype resembled that seen after interspecies crosses in Rhododendron, Escobar-Restrepo et al. tested whether crosses with A. thaliana relatives would yield similar phenotypes and thereby implicate FERONIA in interspecies barriers. Indeed, crosses of A. thaliana females with Cardamine flexuosa pollen or with pollen of a more closely related species, Arabidopsis lyrata, yielded a pollen tube overgrowth phenotype. Recent studies suggest that synergid cells secrete a pollen tube attractant (5-7). In addition, an ovule already targeted by a pollen tube may produce a repellent to ward off additional pollen tubes (7). Moreover, these attractants and repellents exhibit some degree of species specificity (7, 8). In both sirène and feronia mutant plants, some ovules attracted more than one pollen tube (2, 3), perhaps because the attractant persists when the first pollen tube does not burst.

Proteins involved in sexual recognition can show amino acid diversification in regions that interact with a protein from the other sex (9) as the proteins evolve to match each other; that is, genes with increased rates of evolution increase the frequency with which incompatibilities evolve between closely relatedspecies. Among plants related to A. thaliana, the extracellular domain of FERONIA has more nonsynonymous nucleotide changes than the highly conserved kinase domain. This suggests that the presumed ligand-binding region was subject to positive selection and that coevolution between FERONIA and an equivalently diverging ligand could contribute to reproductive isolation.

Escobar-Restrepo et al. propose a signaling pathway wherein ligand from the pollen tube interacts with FERONIA, causing the synergid cell to send another signal back to the pollen tube to stop growing and burst (see the figure). Much more information is needed to test this intriguing model. The immediate challenge is to identify the FERONIA ligand. There is no way to guess a priori what it might be; even within the LRR (leucine-rich repeat) receptor kinase group—the best-studied such group in plants—the known ligands are diverse (10). Potential ligand-receptor pairs might be identified through screens of mutant plants for similar phenotypes (11) such as pollen tube overgrowth. Yeast two-hybrid screens (12) are another option, in which the extracellular domain of FERONIA can be used as bait for complementary DNA libraries prepared from germinated pollen tubes.

It will also be important to determine whether disruptions of FERONIA homologs in other species give similar phenotypes; if so, the pollen overgrowth phenotype may occur with interspecies crosses in other plant families. It is intriguing that in the cross with A. lyrata, 50% of the pollinated A. thaliana ovules showed the pollen overgrowth phenotype, whereas the other 50% showed normal fertilization (1). Indeed, interspecies crosses with A. lyrata are possible (13). Escobar-Restrepo et al. suggest that there might be different isoforms of the ligand in A. lyrata, with one allelic variant that recognizes the A. thaliana version of FERONIA.

FERONIA and its upstream and downstream signaling partners may be the key to successful sperm discharge. If so, then manipulating the components of this pathway might facilitate more promiscuous hybridizations than occur in nature.

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