Dataset Information

New opportunities and insights into Papaver self-incompatibility by imaging engineered Arabidopsis pollen.

ABSTRACT: Pollen tube growth is essential for plant reproduction. Their rapid extension using polarized tip growth provides an exciting system for studying this specialized type of growth. Self-incompatibility (SI) is a genetically controlled mechanism to prevent self-fertilization. Mechanistically, one of the best-studied SI systems is that of Papaver rhoeas (poppy). This utilizes two S-determinants: stigma-expressed PrsS and pollen-expressed PrpS. Interaction of cognate PrpS-PrsS triggers a signalling network, causing rapid growth arrest and programmed cell death (PCD) in incompatible pollen. We previously demonstrated that transgenic Arabidopsis thaliana pollen expressing PrpS-green fluorescent protein (GFP) can respond to Papaver PrsS with remarkably similar responses to those observed in incompatible Papaver pollen. Here we describe recent advances using these transgenic plants combined with genetically encoded fluorescent probes to monitor SI-induced cellular alterations, including cytosolic calcium, pH, the actin cytoskeleton, clathrin-mediated endocytosis (CME), and the vacuole. This approach has allowed us to study the SI response in depth, using multiparameter live-cell imaging approaches that were not possible in Papaver. This lays the foundations for new opportunities to elucidate key mechanisms involved in SI. Here we establish that CME is disrupted in self-incompatible pollen. Moreover, we reveal new detailed information about F-actin remodelling in pollen tubes after SI.

SUBMITTER: Wang L

PROVIDER: S-EPMC7178406 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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New opportunities and insights into Papaver self-incompatibility by imaging engineered Arabidopsis pollen.

Wang Ludi L Triviño Marina M Lin Zongcheng Z Carli José J Eaves Deborah J DJ Van Damme Daniёl D Nowack Moritz K MK Franklin-Tong Vernonica E VE Bosch Maurice M

Journal of experimental botany 20200401 8

Pollen tube growth is essential for plant reproduction. Their rapid extension using polarized tip growth provides an exciting system for studying this specialized type of growth. Self-incompatibility (SI) is a genetically controlled mechanism to prevent self-fertilization. Mechanistically, one of the best-studied SI systems is that of Papaver rhoeas (poppy). This utilizes two S-determinants: stigma-expressed PrsS and pollen-expressed PrpS. Interaction of cognate PrpS-PrsS triggers a signalling n ...[more]

PMID: 32100005

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Project description:BackgroundPollen-pistil interactions are an essential prelude to fertilization in angiosperms and determine compatibility/incompatibility. Pollen-pistil interactions have been studied at a molecular and cellular level in relatively few families. Self-incompatibility (SI) is the best understood pollen-pistil interaction at a molecular level where three different molecular mechanisms have been identified in just five families. Here we review studies of pollen-pistil interactions and SI in the Asteraceae, an important family that has been relatively understudied in these areas of reproductive biology.ScopeWe begin by describing the historical literature which first identified sporophytic SI (SSI) in species of Asteraceae, the SI system later identified and characterized at a molecular level in the Brassicaceae. Early structural and cytological studies in these two families suggested that pollen-pistil interactions and SSI were similar, if not the same. Recent cellular and molecular studies in Senecio squalidus (Oxford ragwort) have challenged this belief by revealing that despite sharing the same genetic system of SSI, the Brassicaceae and Asteraceae molecular mechanisms are different. Key cellular differences have also been highlighted in pollen-stigma interactions, which may arise as a consequence of the Asteraceae possessing a 'semi-dry' stigma, rather than the 'dry' stigma typical of the Brassicaceae. The review concludes with a summary of recent transcriptomic analyses aimed at identifying proteins regulating pollen-pistil interactions and SI in S. squalidus, and by implication the Asteraceae. The Senecio pistil transcriptome contains many novel pistil-specific genes, but also pistil-specific genes previously shown to play a role in pollen-pistil interactions in other species.ConclusionsStudies in S. squalidus have shown that stigma structure and the molecular mechanism of SSI in the Asteraceae and Brassicaceae are different. The availability of a pool of pistil-specific genes for S. squalidus offers an opportunity to elucidate the molecular mechanisms of pollen-pistil interactions and SI in the Asteraceae.

Project description:In angiosperms, self-incompatibility (SI) is a common and widespread mechanism for plant prevention of inbreeding, and late-acting self-incompatibility (LSI) may be ancestral in the group. In this work, we studied Schima superba, a species in Theaceae that is a commercially important timer and fire-resistant tree, and revealed its LSI mechanism. Hormones, enzymes, transcriptomes, and proteins were compared between self-pollination (SP) and outcross pollination (OP) in the styles and ovaries from 0 to 120 h after pollination. The self-pollen tubes grew to the bottom of the style and entered the ovary within 48 h but failed to penetrate the ovule. Meanwhile, the hormone and peroxidase levels dramatically changed. Transcriptome and proteome analyses explored the molecular mechanisms of LSI and candidate genes related to LSI in S. superba. Overall, 586.71 million reads were obtained, and 79,642 (39.08%) unigenes were annotated. KEGG and GO analysis showed that there were 4531 differentially expressed genes (DEGs) and 82 differentially expressed proteins (DEPs) at 48 h in self- (SP) versus outcross pollination (OP). Among these, 160 DEGs and 33 DEPs were involved in pollen-pistil interactions. "Pollen-pistil interaction," "signal recognition," and "component of membrane" were downregulated in SP, whereas "cell wall and membrane biosynthetic process," and "oxidoreductase activity" were upregulated. The DEGs involved with S-RNases and SCF during SP suggested that the LSI occurred at 48 h in the ovary and that the LSI in S. superba was under gametophyte control. Calcium ion increase and release, mitochondrial function loss, and ROS disruption further aggravated PCD progress and cell death. The LSI of S. superba, which happened 48 h after pollination, was a key time point. The incompatibility PT ceased growth in the ovary because of S-RNase recognition and PCD in this organ. This study highlights the LSI molecular mechanism in S. superba and provides a reference to other species in Theaceae.

Dataset Information

New opportunities and insights into Papaver self-incompatibility by imaging engineered Arabidopsis pollen.

Publications

New opportunities and insights into Papaver self-incompatibility by imaging engineered Arabidopsis pollen.

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