Transcriptional Characteristics and Differences in Arabidopsis Stigmatic Papilla Cells Pre- and Post-Pollination

Abstract

Pollination is an important early step in sexual plant reproduction. In Arabidopsis thaliana, sequential pollination events, from pollen adhesion onto the stigma surface to pollen tube germination and elongation, occur on the stigmatic papilla cells. Following successful completion of these events, the pollen tube penetrates the stigma and finally fertilizes a female gametophyte. The pollination events are thought to be initiated and regulated by interactions between papilla cells and pollen. Here, we report the characterization of gene expression profiles of unpollinated (UP), compatible pollinated (CP) and incompatible pollinated (IP) papilla cells in A. thaliana. Based on cell type-specific transcriptome analysis from a combination of laser microdissection and RNA sequencing, 15,475, 17,360 and 16,918 genes were identified as expressed in UP, CP and IP papilla cells, respectively, and, of these, 14,392 genes were present in all three data sets. Differentially expressed gene (DEG) analyses identified 147 and 71 genes up-regulated in CP and IP papilla cells, respectively, and 115 and 46 genes down-regulated. Gene Ontology and metabolic pathway analyses revealed that papilla cells play an active role as the female reproductive component in pollination, particularly in information exchange, signal transduction, internal physiological changes and external morphological modification. This study provides fundamental information on the molecular mechanisms involved in pollination in papilla cells, furthering our understanding of the reproductive role of papilla cells.

Time-Course Transcriptome Analysis of Compatible and Incompatible Pollen-Stigma Interactions in Brassica napus L.

“…Thus, genes related to tubulin binding might regulate self-pollen rejection by affecting the stability of MT network. In addition, compared to previous studies, a quantity of DEGs were also represented here, such as genes related to jasmonic acid production and plant-type cell wall metabolism were up-regulated at late stage in UP vs. PC samples, which is consistent with results reported by Swanson et al (2005) and Matsuda et al (2014). Most genes involved in stress response or defense response were up-regulated in both incompatible and compatible reactions at late-time points (20 and 30 min after pollination), while the unique proteins in the same GO terms were found to be down-regulated in incompatible pollination previously (Samuel et al, 2011).…”

“…A total of 37 metabolic pathways were identified. Starch and sucrose metabolism is one of the three most over-represented metabolic pathways, which has been reported by Matsuda et al (2014). Biosynthesis of antibiotics, and cysteine and methionine metabolism pathways are first annotated in this study.…”

“…Through proteomic analysis of stigmatic proteins following incompatible pollination in B. napus , 19 down-regulated unique candidate proteins were identified specially in SI (Samuel et al, 2011). Matsuda et al (2014) applied laser microdissection (LM) and RNA sequencing (RNA-seq) to detect the cell type-specific transcriptome in Brassicaceae papillae cells and characterized gene expression 1 h after compatible and incompatible pollination. Although these studies contributed to our understanding of the molecular mechanisms related to pollen-stigma interactions, the consecutive changes of gene expression and dynamic molecular activities during the early stages (within 30 min) of pollination remained to be revealed.…”

Pollen Aquaporins: The Solute Factor

“…Considering AtPIP1;4 was found to be up-regulated in stigmas upon compatible pollination (Matsuda et al, 2015) and has a role in H 2 O 2 transport for signal transduction in immunity pathways (Tian et al, 2016), we could speculate a role of this AQP in ROS signaling during pollination.…”

“…Comparative analysis of pistil transcriptomes revealed the expression of PIP1 and PIP2 in species with dry and semi-dry stigmas ( Oryza sativa, Crocus sativus, Arabidopsis thaliana , and S. squalidus ), but not with wet stigmas ( Nicotiana tabacum ) (Allen et al, 2010). Recently, stigmatic papilla cells transcriptome analysis in A. thaliana ecotype Oldenburg (Old-1), which still retains the female SI function, showed that PIP1;4 is up-regulated in compatible pollinations (using wild-type Old-1 pollen), whereas PIP2;1 and PIP2;7 are down-regulated in incompatible pollinations (using transgenic self-incompatible Old-1 pollen) (Matsuda et al, 2015). These studies support the hypothesis of pistil AQP s potentially regulating pollen hydration in dry stigmas but not in wet stigmas, since the presence of the stigmatic exudate obviates the control of water flow to pollen grains.…”