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Title: Integrating Membrane Transport with Male Gametophyte Development and Function through Transcriptomics.

Abstract

Male fertility depends on the proper development of the male gametophyte, successful pollen germination, tube growth and delivery of the sperm cells to the ovule. Previous studies have shown that nutrients like boron, and ion gradients or currents of Ca2+, H+, and K+ are critical for pollen tube growth. However, the molecular identities of transporters mediating these fluxes are mostly unknown. As a first step to integrate transport with pollen development and function, a genome-wide analysis of transporter genes expressed in the male gametophyte at four developmental stages was conducted. About 1269 genes encoding classified transporters were collected from the Arabidopsis thaliana genome. Of 757 transporter genes expressed in pollen, 16% or 124 genes, including AHA6, CNGC18, TIP1.3 and CHX08, are specifically or preferentially expressed relative to sporophytic tissues. Some genes are highly expressed in microspores and bicellular pollen (COPT3, STP2, OPT9); while others are activated only in tricellular or mature pollen (STP11, LHT7). Analyses of entire gene families showed that a subset of genes, including those expressed in sporophytic tissues, were developmentally-regulated during pollen maturation. Early and late expression patterns revealed by transcriptome analysis are supported by promoter::GUS analyses of CHX genes and by other methods. Recent genetic studiesmore » based on a few transporters, including plasma membrane H+ pump AHA3, Ca2+ pump ACA9, and K+ channel SPIK, further support the expression patterns and the inferred functions revealed by our analyses. Thus, revealing the distinct expression patterns of specific transporters and unknown polytopic proteins during microgametogenesis provides new insights for strategic mutant analyses necessary to integrate the roles of transporters and potential receptors with male gametophyte development.« less

Authors:
; ; ; ; ; ; ;
Publication Date:
Research Org.:
University of Maryland, College Park, MD
Sponsoring Org.:
USDOE - Office of Energy Research (ER)
OSTI Identifier:
932549
Report Number(s):
DOE/ER/20200-2
DOE Contract Number:
FG02-95ER20200
Resource Type:
Journal Article
Resource Relation:
Journal Name: Plant Physiology; Journal Volume: 140
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Systems biology, membrane transport, Arabidopsis thaliana, genomics, pollen, transcriptome

Citation Formats

Bock KW, D Honys, JM. Ward, S Padmanaban, EP Nawrocki, KD Hirschi, D Twell, and H Sze. Integrating Membrane Transport with Male Gametophyte Development and Function through Transcriptomics.. United States: N. p., 2006. Web. doi:10.1104/pp.105.074708.
Bock KW, D Honys, JM. Ward, S Padmanaban, EP Nawrocki, KD Hirschi, D Twell, & H Sze. Integrating Membrane Transport with Male Gametophyte Development and Function through Transcriptomics.. United States. doi:10.1104/pp.105.074708.
Bock KW, D Honys, JM. Ward, S Padmanaban, EP Nawrocki, KD Hirschi, D Twell, and H Sze. Sun . "Integrating Membrane Transport with Male Gametophyte Development and Function through Transcriptomics.". United States. doi:10.1104/pp.105.074708.
@article{osti_932549,
title = {Integrating Membrane Transport with Male Gametophyte Development and Function through Transcriptomics.},
author = {Bock KW and D Honys and JM. Ward and S Padmanaban and EP Nawrocki and KD Hirschi and D Twell and H Sze},
abstractNote = {Male fertility depends on the proper development of the male gametophyte, successful pollen germination, tube growth and delivery of the sperm cells to the ovule. Previous studies have shown that nutrients like boron, and ion gradients or currents of Ca2+, H+, and K+ are critical for pollen tube growth. However, the molecular identities of transporters mediating these fluxes are mostly unknown. As a first step to integrate transport with pollen development and function, a genome-wide analysis of transporter genes expressed in the male gametophyte at four developmental stages was conducted. About 1269 genes encoding classified transporters were collected from the Arabidopsis thaliana genome. Of 757 transporter genes expressed in pollen, 16% or 124 genes, including AHA6, CNGC18, TIP1.3 and CHX08, are specifically or preferentially expressed relative to sporophytic tissues. Some genes are highly expressed in microspores and bicellular pollen (COPT3, STP2, OPT9); while others are activated only in tricellular or mature pollen (STP11, LHT7). Analyses of entire gene families showed that a subset of genes, including those expressed in sporophytic tissues, were developmentally-regulated during pollen maturation. Early and late expression patterns revealed by transcriptome analysis are supported by promoter::GUS analyses of CHX genes and by other methods. Recent genetic studies based on a few transporters, including plasma membrane H+ pump AHA3, Ca2+ pump ACA9, and K+ channel SPIK, further support the expression patterns and the inferred functions revealed by our analyses. Thus, revealing the distinct expression patterns of specific transporters and unknown polytopic proteins during microgametogenesis provides new insights for strategic mutant analyses necessary to integrate the roles of transporters and potential receptors with male gametophyte development.},
doi = {10.1104/pp.105.074708},
journal = {Plant Physiology},
number = ,
volume = 140,
place = {United States},
year = {Sun Jan 01 00:00:00 EST 2006},
month = {Sun Jan 01 00:00:00 EST 2006}
}
  • Recombinant cDNA libraries to poly(A)RNA isolated from mature pollen of Zea mays and Tradescantia paludosa have been constructed. Northern blot analyses indicate that several of the clones are unique to pollen and are not expressed in vegetative tissues. The majority, however, are expressed both in pollen and vegetative tissues. Southern hybridizations show that the pollen specific sequences in corn are present in one or a very few copies in the genome. By using several of the clones as probes, it was found that there are at least two different groups of mRNAs with respect to their synthesis. The mRNAs ofmore » the first group represented by the pollen specific clones are synthesized after microspore mitosis and increase in concentration up to maturity. The second group, exemplified by actin mRNA, begins to accumulate soon after meiosis, reaches its maximum by later pollen interphase, and decreases thereafter. Although the actin mRNA and the pollen specific mRNAs studied show very different patterns of initiation of synthesis and accumulation during pollen development, the rates of decline in these mRNAs during the first 60 minutes of germination and pollen tube growth in Tradescantia are similar and reflect the previously observed declines in rates of protein synthesis during this period.« less
  • Three pairs of isonuclear lines of cytoplasmic male sterile (CMS) and fertile Petunia cells (Petunia hybrida (Hook) Vilm. and Petunia parodii L.S.M.) grown in suspension culture were examined for sensitivity to inhibitors of respiratory electron transport at time-points after transfer into fresh media. Cells from CMS lines differed from cells of fertile lines in their utilization of the cyanide-insensitive oxidase pathway. Under our culture regime, after approximately 3 days of culture cells from the CMS lines exhibited much lower cyanide-insensitive, salicylhydoxamic acid-sensitive respiration than cells from the fertile lines. This respiratory difference was shown to be specific to the mitochondrialmore » alternative oxidase pathway by using other characteristic inhibitors of mitochondrial electron transport in experiments with isolated mitochondria. Immature anthers from CMS plants also showed lower alternative oxidase activity relative to anthers from male fertile plants, but no such difference was detected in leaf tissue, ovary or perianth tissue, or anthers collected just prior to anthesis. A cell line from a fertile plant carrying a nuclear fertility restorer gene and the CMS cytoplasm exhibited increased activity of the alternative pathway compared with the CMS lines.« less
  • Red cell cation transports (Na(+)-K+ pump, Na(+)-K+ cotransport system, Na(+)-Li+ countertransport, and Na+ and K+ passive permeabilities) and blood and hair lead levels were measured in 129 healthy adult Caucasians not occupationally exposed to lead. In agreement with previously reported in vitro results showing a lead-induced Na(+)-K+ ATPase inhibition, Na(+)-K+ pump activity was inversely correlated with hair lead (r = -0.18, P less than 0.05); it was not significantly correlated with blood lead. Na(+)-K+ cotransport activity was inversely correlated with blood lead contents (r = -0.23, P less than 0.05) but not with hair lead. No significant correlation was foundmore » between the remaining cation transport pathways and lead levels. It is hypothesized that environmental, long-term exposure to lead may result in pump inhibition, while a recent exposition to lead may result in inhibition of the Na(+)-K+ cotransport system. Further research is required in order to determine if red cell Na(+)-K+ pump and Na(+)-K+ cotransport activities are sensitive indicators of chronic and recent exposures to lead, respectively.« less