Pollination in species with dry stigmas: the nature of the early stigmatic response and the pathway taken by pollen tubes

Abstract

SUMMARYInteraction between the pollen grain, pollen tube and the stigma surface has been studied in five species regarded as possessing dry stigma surfaces; Brassica oleracea L., Arabidopsis thaliana (L.), Heynh, Papaver rhoeas L., Cosmos bipinnatus Cav. and Helianthus annuus L.In B. oteracea and A. thaliana, stigmatic response to pollination includes events in the papillar cytoplasm and changes to the stigmatic surface beneath the grain. In particular a specialized outer element of the cell wall expands prior to pollen tube penetration. The pollen tube, which enters through a ' foot' of pollen coating, grows in a space generated between an inner and the outer element of the wall and extends to the base of the papilla where it enters the middle lamellae of the subjacent cell layer. However, in A. thaliana tubes frequently were seen to penetrate all components of the stigmatic cell wall, an event only previously recorded in immature stigmas of B. oleracea. In self pollinations of self-incompatible B. oleracea involving strong S (incompatibility) alleles no changes take place in the papillar cell wall.In P. rhoeas the stigmatic surface responds to self and cross pollination by the secretion of electron-lucent material beneath the cuticle, causing it to become detached from the outer surface of the stigmatic cell wall. The pollen tubes then penetrate the cuticle and grow towards the base of the papilla in the space thus generated. The tubes continue to grow intercellularly in the transmitting tissue which lies horizontally in rays beneath the papillae.In members of the Compositae, C bipinnatus and H. annuus, both stigma and pollen respond to pollination by producing copious quantities of an electron-opaque matrix, which frequently causes individual papillae to adhere together. Pollen tubes, which are formed following both compatible and incompatible intraspecific pollinations, grow into this matrix and toward the base of the papillae. There, in common with the other plants studied, they grow intercellularly and enter the transmitting tissue of the style.These findings are discussed in the light of current views of the mechanisms operating during angiosperm pollination and of the significance of the stigmatic response to the functioning of self-incompatibility mechanisms.

Signaling Events in Pollen Acceptance or Rejection in the Arabidopsis Species

“…Arabidopsis species possesses a dry stigma that is covered with papillae on the stigmatic surface. Once a compatible pollen grain comes in contact with a stigmatic papilla, the early stages of pollen capture and adhesion, pollen hydration, and germination are closely regulated (Elleman et al 1992 ;Preuss et al 1993 ;Kandasamy et al 1994 ;Zinkl et al 1999 ). The ability to conduct genetic screens with relative ease in A. thaliana has aided in identifying a number of factors that regulate pollen-stigma interactions (Preuss et al 1993 ;Hulskamp et al 1995 ;Nishikawa et al 2005 ).…”

“…Following pollination, two components of the pollen grain come in contact with the stigmatic papilla: the exine, which is the sculptured outermost layer of the pollen grain, and the lipid-and protein-rich pollen coat that is present in the pockets of the exine (Elleman et al 1992 ;Kandasamy et al 1994 ). The initial binding of compatible A. thaliana pollen to the stigmatic papilla was determined to be mediated by the pollen exine , while the pollen coat was not required (Zinkl et al 1999 ).…”

“…The pollen coat is then involved in further adhesion of the pollen grain to the stigmatic papilla. At this stage, the pollen coat fl ows out from the pollen grain toward the stigmatic papilla to mix with the lipidic and proteinaceous surface of the stigmatic papilla, creating a more robust connection at the pollen-stigma interface (Elleman et al 1992 ;Preuss et al 1993 ;Kandasamy et al 1994 ;Zinkl et al 1999 ).…”

“…Although the molecular mechanism of water transfer from the stigmatic papilla to the pollen grain has yet to be determined, changes to the impermeable pollen coat with the formation of the pollen-stigma interface are proposed to create a passageway for water to fl ow from the stigma to the pollen grain (Elleman and Dickinson 1986 ;Elleman et al 1992 ;Murphy 2006 ). This may involve changes in the lipid properties of the pollen-stigma interface through the actions of lipid-binding oleosin-like proteins or lipases that have been identifi ed in the A. thaliana pollen coat (Mayfi eld et al 2001 ).…”

“…Changes at the A. thaliana stigmatic surface were observed after compatible pollen attachment, including the expansion of the outer layer of the cell wall beneath the grain (Elleman et al 1992 ;Kandasamy et al 1994 ). In B. oleracea , the expansion of the outer layer of the stigmatic cell wall appears to be initiated by factors in the pollen coating as application of isolated pollen coat extracts to the stigma was found to cause cell wall expansion (Elleman and Dickinson 1996 ).…”