Time-lapse imaging of self- and cross-pollinations in Brassica rapa

Hiroi, Kenichiro; Sone, Mikako; Sakazono, Satomi; Osaka, Mariko; Masuko-Suzuki, Hiromi; Matsuda, Tomoki; Suzuki, Go; Suwabe, Keita; Watanabe, Masao

doi:10.1093/aob/mct102

Cited by 25 publications

(23 citation statements)

References 40 publications

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“…Thus, inhibition of the incompatible pollen acts very early, within the first minutes following stigma contact, blocking pollen hydration. As previously described, hydration appears as the first check point controlling pollen rejection in SI species with dry stigma (Zuberi and Dickinson, 1985; Dickinson, 1995; Samuel et al , 2009; Hiroi et al , 2013; Safavian and Goring, 2013; Wang et al , 2016). In this study, the hydration threshold required to trigger germination was found to correspond to a pollen L/W ratio below 1.4.…”

Section: Discussionmentioning

confidence: 64%

“…Because the increase of water content in pollen grain is correlated with change of its shape from ellipsoid to spheroid (Zuberi and Dickinson, 1985; Hiroi et al , 2013; Wang et al , 2016), for each pollen grain, we recorded every two minutes the ratio between the long and the wide axis (L/W) to estimate the pollen hydration rate until germination. Slopes were determined by linear regression of the hydration curve based on pollen ratio evolution during the first 10 minutes period (5 data points), using the curve f = ax + b.…”

Section: Methodsmentioning

confidence: 99%

“…This interaction induces SRK phosphorylation and activation of the signaling cascade leading to self-pollen rejection (Cabrillac et al , 2001). Incompatible pollen grains fail to hydrate properly and do not germinate or only germinate a short pollen tube whose growth is arrested on papilla cells (Dickinson, 1995; Hiroi et al , 2013). Although Arabidopsis thaliana is self-fertile, transgenic SI A. thaliana lines were generated by reintroducing SCR/SP11 and SRK gene pairs from its SI close relative A. lyrata (Nasrallah and Nasrallah, 2002; Nasrallah et al , 2004).…”

Section: Introductionmentioning

confidence: 99%

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Live-cell imaging of early events following pollen perception in self-incompatibleArabidopsis thaliana

Rozier

Riglet

Kodera

et al. 2019

Preprint

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Early events occurring at the surface of the female organ are critical for plant reproduction, especially in species with a dry stigma. Following landing on the stigmatic papilla cells, the pollen hydrates and germinates a tube, which penetrates the cell wall and grows towards the ovules to convey the male gametes to the embryo sac. In self-incompatible (SI) species within the Brassicaceae, these processes are blocked when the stigma encounters an incompatible pollen. Here, based on the generation of SI-Arabidopsis lines and by setting up a live imaging system, we showed that control of pollen hydration has a central role in pollen selectivity. The faster pollen pumps water from the papilla during an initial period of 10 minutes, the faster it germinates. Furthermore, we found that the SI barriers act to block the proper hydration of incompatible pollen and when hydration is promoted by high humidity, an additional control prevents pollen tube penetration into the stigmatic wall. In papilla cells, actin bundles focalize at the contact site with the compatible pollen but not with the incompatible one, raising the possibility that stigmatic cells react to the mechanical pressure applied by the invading growing tube.HighlightA live imaging system coupled with self-incompatible Arabidopsis lines highlight the role of stigmatic cells in controlling pollen hydration and in reacting to pollen tube intrusion by remodeling actin cytoskeleton.

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Section: Discussionmentioning

confidence: 64%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Live-cell imaging of early events following pollen perception in self-incompatibleArabidopsis thaliana

Rozier

Riglet

Kodera

et al. 2019

Preprint

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“…In this system compatibility is established at the stigma surface within minutes of pollination when compatible grains gain access to stigmatic water, but incompatible pollen generally fail to fully hydrate and germinate. Thus, pollen hydration on the stigma surface is essential for successful reproduction and is a strictly regulated checkpoint centred in the stigma (Dickinson, 1995;Ma et al, 2012;Hiroi et al, 2013). Possession of a dry stigma comes with the requirement that the exine surface of conspecific pollen must carry a coating (tryphine) (Dickinson, 1995;Dickinson et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

PCP‐B class pollen coat proteins are key regulators of the hydration checkpoint in Arabidopsis thaliana pollen–stigma interactions

et al. 2016

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Summary The establishment of pollen–pistil compatibility is strictly regulated by factors derived from both male and female reproductive structures. Highly diverse small cysteine‐rich proteins (CRPs) have been found to play multiple roles in plant reproduction, including the earliest stages of the pollen–stigma interaction. Secreted CRPs found in the pollen coat of members of the Brassicaceae, the pollen coat proteins (PCPs), are emerging as important signalling molecules that regulate the pollen–stigma interaction.Using a combination of protein characterization, expression and phylogenetic analyses we identified a novel class of Arabidopsis thaliana pollen‐borne CRPs, the PCP‐Bs (for pollen coat protein B‐class) that are related to embryo surrounding factor (ESF1) developmental regulators. Single and multiple PCP‐B mutant lines were utilized in bioassays to assess effects on pollen hydration, adhesion and pollen tube growth.Our results revealed that pollen hydration is severely impaired when multiple PCP‐Bs are lost from the pollen coat. The hydration defect also resulted in reduced pollen adhesion and delayed pollen tube growth in all mutants studied.These results demonstrate that At PCP‐Bs are key regulators of the hydration ‘checkpoint’ in establishment of pollen–stigma compatibility. In addition, we propose that interspecies diversity of PCP‐Bs may contribute to reproductive barriers in the Brassicaceae.

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“…Papilla cells have various roles in this step, such as discrimination of pollen grains for inter- and intraspecies barriers, pollen hydration, supply of stigmatic resources for pollen germination and pollen tube elongation, and pollen tube guidance (de Nettancourt 2001, Goto et al 2011). However, the molecular basis of these mechanisms of pollination is still largely unclear (Hiroi et al 2013). …”

Section: Introductionmentioning

confidence: 99%

Cell Type-Specific Transcriptome of Brassicaceae Stigmatic Papilla Cells From a Combination of Laser Microdissection and RNA Sequencing

Osaka

Matsuda

Sakazono

et al. 2013

Plant and Cell Physiology

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Pollination is an early and critical step in plant reproduction, leading to successful fertilization. It consists of many sequential processes, including adhesion of pollen grains onto the surface of stigmatic papilla cells, foot formation to strengthen pollen–stigma interaction, pollen hydration and germination, and pollen tube elongation and penetration. We have focused on an examination of the expressed genes in papilla cells, to increase understanding of the molecular systems of pollination. From three representative species of Brassicaceae (Arabidopsis thaliana, A. halleri and Brassica rapa), stigmatic papilla cells were isolated precisely by laser microdissection, and cell type-specific gene expression in papilla cells was determined by RNA sequencing. As a result, 17,240, 19,260 and 21,026 unigenes were defined in papilla cells of A. thaliana, A. halleri and B. rapa, respectively, and, among these, 12,311 genes were common to all three species. Among the17,240 genes predicted in A. thaliana, one-third were papilla specific while approximately half of the genes were detected in all tissues examined. Bioinformatics analysis revealed that genes related to a wide range of reproduction and development functions are expressed in papilla cells, particularly metabolism, transcription and membrane-mediated information exchange. These results reflect the conserved features of general cellular function and also the specific reproductive role of papilla cells, highlighting a complex cellular system regulated by a diverse range of molecules in these cells. This study provides fundamental biological knowledge to dissect the molecular mechanisms of pollination in papilla cells and will shed light on our understanding of plant reproduction mechanisms.

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Time-lapse imaging of self- and cross-pollinations in Brassica rapa

Abstract: Regulated hydration of pollen is a key process for both pollination and self-incompatibility, and this is achieved by a balanced complex of hydration, dehydration and nutrient supply to pollen grains from stigmatic papilla cells.

Cited by 25 publications

References 40 publications

Live-cell imaging of early events following pollen perception in self-incompatibleArabidopsis thaliana

Live-cell imaging of early events following pollen perception in self-incompatibleArabidopsis thaliana

PCP‐B class pollen coat proteins are key regulators of the hydration checkpoint in Arabidopsis thaliana pollen–stigma interactions

Cell Type-Specific Transcriptome of Brassicaceae Stigmatic Papilla Cells From a Combination of Laser Microdissection and RNA Sequencing

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