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Title: Integrating membrane transport with male gametophyte development and function through transcriptomics(1)[W]

Author
item BOCK, KEVIN - UNIV OF MARYLAND-COL PARK
item HONYS, DAVID - INSTITUTE EXPMTL BOTANY
item WARD, JOHN - UNIV OF MINNESOTA-ST PAUL
item PADMANABAN, SENTHILKUMAR - UNIV OF MARYLAND-COL PARK
item NAWROCKI, ERIC - UNIV OF MARYLAND-COL PARK
item Hirschi, Kendal
item TWELL, DAVID - UNIV OF LEICESTER, UK
item SZE, HEVEN - UNIV OF MARYLAND-COL PARK

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/13/2006
Publication Date: 4/11/2006
Citation: Bock, K.W., Honys, D., Ward, J.M., Padmanaban, S., Nawrocki, E.P., Hirschi, K.D., Twell, D., Sze, H. 2006. Integrating membrane transport with male gametophyte development and function through transcriptomics(1)[W]. Plant Physiology. 140(4):1151-1168.

Interpretive Summary: Plant reproduction depends on the development of pollen and ovules--the plant's equivalent of sexual organs. We want to be able to understand the biology of plant reproduction in order to manipulate these events. Here we have analyzed which different sets of DNA are turned on during the creation of the plant's reproductive system. We have discovered that plant transporters, which move different nutrients across biological membranes, are turned on during these events. We have analyzed a large data set and shown that at specific times, hundreds of these transporters are active. These observations will aid in our attempts to further understand this intricate biological process.

Technical 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 Ca(2+), 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. Approximately 1,269 genes encoding classified transporters were collected from the Arabidopsis (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, was developmentally regulated during pollen maturation. Early and late expression patterns revealed by transcriptome analysis are supported by promoter::“Beta”-glucuronidase analyses of "CHX" genes and by other methods. Recent genetic studies based on a few transporters, including plasma membrane H(+) pump AHA3, Ca(2+) 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.