Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis

Abstract

Sexual reproduction in plants requires elongation of the pollen tube through the transmitting tissues toward the ovary. Tube growth rate is a major determinant of pollen competitive ability. We report that a K⁺ channel of the Shaker family in Arabidopsis, SPIK, plays an important role in pollen tube development. SPIK was found to be specifically expressed in pollen. When SPIK was heterologously expressed in COS cells, its product formed hyperpolarization-activated K⁺ channels. Disruption (T-DNA insertion) of the SPIK coding sequence strongly affected inwardly rectifying K⁺-channel activity in the pollen-grain plasma membrane. Measurements of membrane potential in growing pollen tubes yielded data compatible with a contribution of SPIK to K⁺ influx. In vitro pollen germination assays were performed, revealing that the disruption results in impaired pollen tube growth. Analysis of the transmission rate of the disrupted allele in the progeny of heterozygous plants revealed a decrease in pollen competitive ability, the probability of fertilization by mutant pollen being ∼1.6 times lower than that by wild-type pollen. The whole set of data supports the hypothesis that functional expression ofSPIK plays a role in K⁺ uptake in the growing pollen tube, and thereby in tube development and pollen competitive ability.