Pollen performance before and during the autotrophic–heterotrophic transition of pollen tube growth

Abstract

For species with bicellular pollen, the attrition of pollen tubes is often greatest where the style narrows at the transition between stigmatic tissue and the transmitting tissue of the style. In this region, the tubes switch from predominantly autotrophic to predominantly heterotrophic growth, the generative cell divides, the first callose plugs are produced, and, in species with RNase-type self-incompatibility (SI), incompatible tubes are arrested. We review the literature and present new findings concerning the genetic, environmental and stylar influences on the performance of pollen before and during the autotrophic-heterotrophic transition of pollen tube growth. We found that the ability of the paternal sporophyte to provision its pollen during development significantly influences pollen performance during the autotrophic growth phase. Consequently, under conditions of pollen competition, pollen selection during the autotrophic phase is acting on the phenotype of the paternal sporophyte. In a field experiment, using Cucurbita pepo, we found broad-sense heritable variation for herbivore-pathogen resistance, and that the most resistant families produced larger and better performing pollen when the paternal sporophytes were not protected by insecticides, indicating that selection during the autotrophic phase can act on traits that are not expressed by the microgametophyte. In a study of a weedy SI species, Solanum carolinense, we found that the ability of the styles to arrest self-pollen tubes at the autotrophic-heterotrophic transition changes with floral age and the presence of developing fruits. These findings have important implications for selection at the level of the microgametophyte and the evolution of mating systems of plants.

Segregation Analyses of Partial Self-Incompatibility in Self and Cross Progeny of Solanum carolinense Reveal a Leaky S-Allele

“…Our findings, however, are unlikely to be the result of a duplicated pollen determinant of SI because if the pollen component of the S-locus, S-locus F-box protein (Sijacic et al 2004), is duplicated, then an allele carrying such duplication will be rendered fully selfcompatible (Kao and Tsukamoto 2004) and such mutations are not likely to vary the strength of the SI response with floral age or prior fruit development (Good-Avila and Stephenson 2002) as we observed in our previous studies (Stephenson et al 2003;Travers et al 2004). A third possibility involves unlinked modifier genes that may affect the timing or magnitude of the S-RNase expression, its turnover, or the normal function of the SI biochemical pathways (Tsukamoto et al 1999).…”

“…The variation in the strength of SI within and between populations has been reported for a variety of plant species (see Good-Avila and Stephenson 2002;Stephenson et al 2003;Stone et al 2006). For instance, Ando et al (1998) described mixed populations of Petunia axillaris composed of both self-incompatible and self-compatible individuals.…”

“…As with other members of the Solanaceae, S. carolinense displays a typical RNase-mediated gametophytic self incompatibility (GSI) system. In previous studies, we have found that the SI response in S. carolinense is a plastic trait in that self-fertility increases with floral age and when no fruits are produced on the first several inflorescences (Stephenson et al 2003;Travers et al 2004). A series of controlled pollinations were carried out in the greenhouse using plants collected from a large population of horsenettle from Cumberland, Maryland, and we determined that the ability of the styles to arrest self-pollen tubes in the upper style changes with floral age and the presence of developing fruits (Stephenson et al 2003).…”

Floral adaptation and diversification under pollen limitation

“…¼ 0.495 + 0.176, t 46 ¼ 2.87, p , 0.01; figure 3), indicating a weaker influence on fecundity, probably because seed production increases asymptotically with pollen import (Aizen & Harder 2007), but also perhaps because post-pollination processes, such as relaxation of self-incompatibility with flower age (e.g. Stephenson et al 2003), buffer the effects of fragmentation. In general, self-incompatible species experienced stronger effects of fragmentation than selfcompatible species.…”

Defining the Genetic Architecture Underlying Female- and Male-Mediated Nonrandom Mating and Seed Yield Traits in Arabidopsis

“…The genetics of this process have the potential to extend beyond the gametophyte genomes. Heritable differences in pollen tube growth may be encoded by the paternal sporophyte, which preloads pollen grains with nutrients for the initial stages of pollen tube growth, as well as by the male gametophyte genome (Stephenson et al, 2003). If anything, things may be more complex on the female side of the equation.…”