Transcriptional Evidence for Inferred Pattern of Pollen Tube-Stigma Metabolic Coupling during Pollination

Abstract

It is difficult to derive all qualitative proteomic and metabolomic experimental data in male (pollen tube) and female (pistil) reproductive tissues during pollination because of the limited sensitivity of current technology. In this study, genome-scale enzyme correlation network models for plants (Arabidopsis/maize) were constructed by analyzing the enzymes and metabolic routes from a global perspective. Then, we developed a data-driven computational pipeline using the “guilt by association” principle to analyze the transcriptional coexpression profiles of enzymatic genes in the consecutive steps for metabolic routes in the fast-growing pollen tube and stigma during pollination. The analysis identified an inferred pattern of pollen tube-stigma ethanol coupling. When the pollen tube elongates in the transmitting tissue (TT) of the pistil, this elongation triggers the mobilization of energy from glycolysis in the TT cells of the pistil. Energy-rich metabolites (ethanol) are secreted that can be taken up by the pollen tube, where these metabolites are incorporated into the pollen tube's tricarboxylic acid (TCA) cycle, which leads to enhanced ATP production for facilitating pollen tube growth. In addition, our analysis also provided evidence for the cooperation of kaempferol, dTDP-alpha-L-rhamnose and cell-wall-related proteins; phosphatidic-acid-mediated Ca2+ oscillations and cytoskeleton; and glutamate degradation IV for γ-aminobutyric acid (GABA) signaling activation in Arabidopsis and maize stigmas to provide the signals and materials required for pollen tube tip growth. In particular, the “guilt by association” computational pipeline and the genome-scale enzyme correlation network models (GECN) developed in this study was initiated with experimental “omics” data, followed by data analysis and data integration to determine correlations, and could provide a new platform to assist inachieving a deeper understanding of the co-regulation and inter-regulation model in plant research.

Evolutionarily conserved phenylpropanoid pattern on angiosperm pollen

“…photoaffinity-based labeling technologies apparently were unsuccessful in identifying potential interaction partners of the flavonol(glycoside)s [39]. Based on computational enzyme correlation networks there is a recent but unproven hypothesis on the potential role of kaempferol during incorporation of rhamnose into the growing pollen wall in maize [40]. This would suggest a signaling effect of the aglycone, or of a putative degradation product, resulting in downstream effects on the structural properties of the pollen tube, in contrast to recent evidence for a more direct incorporation of HCAAs into the pollen coat [41].…”

UPLCMS/MS-based Untargeted Metabolic Profiling Reveals Changes in the Plumbago auriculata Lam. Metabolome Following Heteromorphic Incompatibility System Interactions

“…Pollen tube growth is a highly energy-consuming process involving many related pathways. After successful recognition, high-energy nutrients must be metabolized to produce acetyl-CoA, which is incorporated into the pollen tube's TCA cycle, ultimately enhancing ATP production to promote pollen tube growth [31]. The superpathway is composed of many metabolites that construct a style metabolic network with annotated pathway information in KEGG.…”

Comprehensive Proteomic Profiling of the Brassica carinata and Triticale Mature Stigma and Pollen

“…However, growth of the pollen tube through the pistil subsequently becomes heterotrophic and depends upon the stigma and style providing nutrients, materials, and energy-rich metabolites to the growing pollen tube for sustained growth and guidance through the pistil to the ovary (McInnis et. al., 2006;Yue et. al., 2014).…”

“…Nucleobasecontaining compounds are involved in a large number of biological processes required for reproduction including the production of pyrimidine nucleotides which are involved in the synthesis and degradation of sucrose (for energy) as well as UDP-glucose which is the precursor for many cell wall polysaccharides needed for cell wall biosynthesis and modification during pollen tube invasion of the pistil (Zrenner et. al., 2006), Ca 2+ and H + fluxes during pollen tube growth through the use of cyclic nucleotide-gated ion channels ), ATP synthesis for the energy required for pollen tube growth, as well as NADPH synthesis as a co-factor for many biological processes, and GDP/GTPcontaining molecules for signaling and cytoskeleton dynamics required for vesicular trafficking during pollen tube growth (Yue et. al., 2014;Cheung and Wu, 2008).…”

“…The Ca 2+ transporters that had elevated protein levels in the triticale stigma could perhaps facilitate this process. Most of the proteins involved in proton transport that increased in abundance, were coupled to ATP synthesis (Table S3.6) which is needed to provide energy rich metabolites to drive pollen tube growth (Yue et. al., 2014).…”