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AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen

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Abstract

Sexual plant reproduction depends on the production and differentiation of functional gametes by the haploid gametophyte generation. Currently, we have a limited understanding of the regulatory mechanisms that have evolved to specify the gametophytic developmental programs. To unravel such mechanisms, it is necessary to identify transcription factors (TF) that are part of such haploid regulatory networks. Here we focus on bZIP TFs that have critical roles in plants, animals and other kingdoms. We report the functional characterization of Arabidopsis thaliana AtbZIP34 that is expressed in both gametophytic and surrounding sporophytic tissues during flower development. T-DNA insertion mutants in AtbZIP34 show pollen morphological defects that result in reduced pollen germination efficiency and slower pollen tube growth both in vitro and in vivo. Light and fluorescence microscopy revealed misshapen and misplaced nuclei with large lipid inclusions in the cytoplasm of atbzip34 pollen. Scanning and transmission electron microscopy revealed defects in exine shape and micropatterning and a reduced endomembrane system. Several lines of evidence, including the AtbZIP34 expression pattern and the phenotypic defects observed, suggest a complex role in male reproductive development that involves a sporophytic role in exine patterning, and a sporophytic and/or gametophytic mode of action of AtbZIP34 in several metabolic pathways, namely regulation of lipid metabolism and/or cellular transport.

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Acknowledgments

Authors thank Dr Milada Čiamporová (Institute of Botany, Slovak Academy of Sciences) and Dr Aleš Soukup (Department of Plant Physiology, Charles University in Prague) for their expertise with evaluation of transmission electron micrographs. Authors gratefully acknowledge financial support from Grant Agency of the Czech Republic (GACR grants 522/06/0896 and 522/09/0858) and Ministry of Education of the Czech Republic (MSMT grant LC06004). DT acknowledges support from the Biotechnology and Biological Sciences Research Council (BBSRC) and the University of Leicester.

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Authors and Affiliations

  1. Laboratory of Pollen Biology, Institute of Experimental Botany ASCR, Rozvojová 263, 165 02, Praha 6, Czech Republic

    Antónia Gibalová, David Reňák, Katarzyna Matczuk, Nikoleta Dupl’áková & David Honys

  2. Department of Plant Physiology, Faculty of Science, Charles University in Prague, Viničná 5, 128 44, Praha 2, Czech Republic

    Antónia Gibalová & David Honys

  3. Faculty of Biological Sciences, Department of Plant Physiology and Anatomy, University of South Bohemia, Branišovská 31, 370 05, Ceske Budejovice, Czech Republic

    David Reňák

  4. Plant Reproduction Lab, Institute of Experimental Botany ASCR, Rozvojová 263, 165 02, Praha 6, Czech Republic

    David Cháb

  5. Department of Biology, University of Leicester, Leicester, LE1 7RH, UK

    David Twell

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  1. Antónia Gibalová
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  2. David Reňák
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  3. Katarzyna Matczuk
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  4. Nikoleta Dupl’áková
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  5. David Cháb
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Correspondence to David Honys.

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Supplementary material 1 (PDF 51 kb)

11103_2009_9493_MOESM2_ESM.xls

Supplementary Table 2 Expression of AtbZIP transcription factors in various tissues and cell types according to aGFP database (Duplakova et al., 2007). (XLS 42 kb)

Supplementary Table 3 List of genes at least two-fold downregulated in atbzip34 pollen (XLS 322 kb)

Supplementary Table 4 List of genes at least two-fold upregulated in atbzip34 pollen (XLS 500 kb)

11103_2009_9493_MOESM5_ESM.xls

Supplementary table 5 List of genes showing late male gametophytic expression profile and at least two-fold downregulated in atbzip34 pollen (XLS 57 kb)

11103_2009_9493_MOESM6_ESM.xls

Supplementary Table 6 List of genes showing late male gametophytic expression profile and at least two-fold upregulated in atbzip34 pollen (XLS 23 kb)

Supplementary material 7 (PDF 65 kb)

11103_2009_9493_MOESM8_ESM.pdf

Supplementary Fig. 1 Transmission electron micrographs of cross-sections of developing male gametophyte from tetrad stage to bicellular pollen. wild type (A, C, E, G, I, K) and atbzip34 (B, D, F, H, J, L). Size bar corresponds to 2 µm (A, B, E-H, J-L) and 5 µm (C, D, I). Tetrad stage (A-D). Tetrads of haploid microspores are surrounded by callose wall and deposits of sporopollenin are visible on surface of outer callose wall in wt (A). Primexine forms characteristic undulations in wt, while the atbzip34 tetrads (B) seem to be younger with smooth plasma membrane and thinner callose wall with no sporopollenin deposits on the outher callosic wall. The structure of tapetum was similar in wt (C) and mutant (D). Uninucleate microspore stage (E-H). Microspores of wt (E) and mutant (F) looked similar with large nucleus and smooth cytoplasm. On the contrary, mutant tapetal cells (H) were less vacuolated than wt (G) and contained clusters of electron-dense granules along the locule wall. Late bicellular stage (I-L). Unlike wt (I), vegetative cell of atbzip34 bicellular pollen (J) was highly vacuolated and was enclosed in characteristic wrinkled intine On the contrary, there were no apparent ultrastructural differences in wt (K) and atbzip34 (L) tapetum; in both genotypes elaioplasts were fully developed. BA, baculae; C, callose wall; E, endothecium; EL, elaioplast; ER, endoplasmic reticulum; GC, generative cell; I, electron-dense inclusions; IN, intine; LO, anther locule; M, middle layer; MS, microspore; N, nucleus; P, plastid; S, starch; T, tapetum; TC, tectum; V, vacuole; VC vegetative cell (PDF 3107 kb)

11103_2009_9493_MOESM9_ESM.pdf

Supplementary Fig. 2 MapMan visualization of genes with altered expression in atbzip34 pollen. General transporters (A), genes involved in development and cell wall and lipid metabolism (B), stress-response genes (C) and metabolic pathways leading to cell wall precursors (C) are shown. Logarithmic scale; downregulated genes in blue, upregulated genes in red (PDF 581 kb)

11103_2009_9493_MOESM10_ESM.pdf

Supplementary Fig. 3 MapMan visualization of transcription factor genes with altered expression in atbzip34 pollen. Logarithmic scale; downregulated genes in blue, upregulated genes in red (PDF 245 kb)

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Gibalová, A., Reňák, D., Matczuk, K. et al. AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen. Plant Mol Biol 70, 581–601 (2009). https://doi.org/10.1007/s11103-009-9493-y

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