Abstract
Key message
Pistil AGPs display dynamic localization patterns in response to fertilization in tomato. SlyFLA9 (Solyc07g065540.1) is a chimeric Fasciclin-like AGP with enriched expression in the ovary, suggesting a potential function during pollen–pistil interaction.
Abstract
During fertilization, the male gametes are delivered by pollen tubes to receptive ovules, deeply embedded in the sporophytic tissues of the pistil. Arabinogalactan glycoproteins (AGPs) are a diverse family of highly glycosylated, secreted proteins which have been widely implicated in plant reproduction, particularly within the pistil. Though tomato (Solanum lycopersicum) is an important crop requiring successful fertilization for production, the molecular basis of this event remains understudied. Here we explore the spatiotemporal localization of AGPs in the mature tomato pistil before and after fertilization. Using histological techniques to detect AGP sugar moieties, we found that accumulation of AGPs correlated with the maturation of the stigma and we identified an AGP subpopulation restricted to the micropyle that was no longer visible upon fertilization. To identify candidate pistil AGP genes, we used an RNA-sequencing approach to catalog gene expression in functionally distinct subsections of the mature tomato pistil (the stigma, apical and basal style and ovary) as well as pollen and pollen tubes. Of 161 predicted AGP and AGP-like proteins encoded in the tomato genome, we identified four genes with specifically enriched expression in reproductive tissues. We further validated expression of two of these, a Fasciclin-like AGP (SlyFLA9, Solyc07g065540.1) and a novel hybrid AGP (SlyHAE, Solyc09g075580.1). Using in situ hybridization, we also found SlyFLA9 was expressed in the integuments of the ovule and the pericarp. Additionally, differential expression analyses of the pistil transcriptome revealed previously unreported genes with enriched expression in each subsection of the mature pistil, setting the foundation for future functional studies.
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taken from Supplementary material Fig. 4, where AGP genes had higher expression in reproductive tissues compared to the rest of the tissues. Color code on the left represents distinct classes of AGPs. Blue: AGP-Extensin hybrid; purple: classical AGP; green: Fasciclin-like AGP; yellow: Lysine-rich AGP. b Protein architecture of Fasciclin-like AGP (SlyFLA9, Solyc07g065540.1) and hybrid AGP-Extensin (SlyHAE, Solyc09g075580.1). c Quantitative RT-PCR of SlyFLA9 and SlyHAE across tomato tissues. Expression values were normalized using SlyACT (Solyc00g017210.1) and SlyUBI (Solyc01g056940.2) as references. FB: 2 mm flower buds. d In situ detection of the SlyFLA9 transcript in a sagittal section of the ovary, dissected from an unpollinated pistil. Left: schematic of the pistil sections shown for reference, middle: antisense probe, right: sense probe; es: embryo sac, se: septum, pl: placenta, ov: ovule, pr: pericarp. Scale bar 50 µm
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Funding
This work was supported by the National Science Foundation under Grant No. IOS-1755482 to CAM. CMLM receives fellowship funding from the Mexican Council of Science and Technology (CONACYT) (773973).
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Sequence data are available from the National Center for Biotechnology Information (NCBI) Sequence Read Archive under project accession number PRJNA721190.
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Communicated by Tetsuya Higashiyama.
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Lara-Mondragón, C.M., MacAlister, C.A. Arabinogalactan glycoprotein dynamics during the progamic phase in the tomato pistil. Plant Reprod 34, 131–148 (2021). https://doi.org/10.1007/s00497-021-00408-1
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DOI: https://doi.org/10.1007/s00497-021-00408-1