Secretory activity is rapidly induced in stigmatic papillae by compatible pollen, but inhibited for self-incompatible pollen in the Brassicaceae.

Daphne R Goring,Darya Safavian,Diane Bassham

doi:10.1371/journal.pone.0084286

Abstract

[In the Brassicaceae, targeted exocytosis to the stigmatic papillar plasma membrane under the compatible pollen grain is hypothesized to be essential for pollen hydration and pollen tube penetration. In contrast, polarized secretion is proposed to be inhibited in the stigmatic papillae during the rejection of self-incompatible pollen. Using transmission electron microscopy (TEM), we performed a detailed time-course of post-pollination events to view the cytological responses of the stigmatic papillae to compatible and self-incompatible pollinations. For compatible pollinations in Arabidopsis thaliana and Arabidopsis lyrata, vesicle secretion was observed at the stigmatic papillar plasma membrane under the pollen grain while Brassica napus stigmatic papillae appeared to use multivesicular bodies (MVBs) for secretion. Exo70A1, a component of the exocyst complex, has been previously implicated in the compatible pollen responses, and disruption of Exo70A1 in both A. thaliana and B. napus resulted in a loss of secretory vesicles/MVBs at the stigmatic papillar plasma membrane. Similarly, for self-incompatible pollinations, secretory vesicles/MVBs were absent from the stigmatic papillar plasma membrane in A. lyrata and B. napus; and furthermore, autophagy appeared to be induced to direct vesicles/MVBs to the vacuole for degradation. Thus, these findings support a model where the basal pollen recognition pathway in the stigmatic papilla promotes exocytosis to accept compatible pollen, and the basal pollen recognition pathway is overridden by the self-incompatibility pathway to prevent exocytosis and reject self-pollen.

Highlights

During the initial stages of pollen-pistil interactions in the Brassicaceae, a basal pollen recognition pathway is activated to allow compatible pollen grains to adhere and germinate on the receptive stigmatic surface of the pistil
The surface of the stigma is covered with stigmatic papillae that come in contact with pollen grains, and pollen hydration is one of the earliest visible signs that a compatible pollen grain has been accepted on Brassicaceae dry stigmas
Exo70A1 was required in the stigmatic papillae for the basal pollen recognition pathway to promote compatible pollen hydration, and so the proposed vesicle secretion would be predicted to be visible during this time [17]

Summary

Introduction

During the initial stages of pollen-pistil interactions in the Brassicaceae, a basal pollen recognition pathway is activated to allow compatible pollen grains to adhere and germinate on the receptive stigmatic surface of the pistil. The stigma can function as a barrier to prevent inappropriate pollen grains, such as foreign pollen or self-incompatible pollen, from germinating on the stigmatic surface (reviewed in [1,2,3]). The surface of the stigma is covered with stigmatic papillae that are coated with a continuous waxy cuticle layer overlaid by proteinaceous pellicle, and these layers are important for the initial pollen contact [4,5,6]. The pollen tube emerges and enters the stigma by growing through the expanded cell wall of the stigmatic papilla [2,5,6]. The pollen discrimination system found in the Brassicaceae rapidly takes place as a result of the reliance of pollen grains on the stigmatic papillae for these early events (reviewed in [1,2])

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