Abstract
ROXY1 and ROXY2 are CC-type floral glutaredoxins with redundant functions in Arabidopsis (Arabidopsis thaliana) anther development. We show here that plants lacking the basic leucine-zipper transcription factors TGA9 and TGA10 have defects in male gametogenesis that are strikingly similar to those in roxy1 roxy2 mutants. In tga9 tga10 mutants, adaxial and abaxial anther lobe development is differentially affected, with early steps in anther development blocked in adaxial lobes and later steps affected in abaxial lobes. Distinct from roxy1 roxy2, microspore development in abaxial anther lobes proceeds to a later stage with the production of inviable pollen grains contained within nondehiscent anthers. Histological analysis shows multiple defects in the anther dehiscence program, including abnormal stability and lignification of the middle layer and defects in septum and stomium function. Compatible with these defects, TGA9 and TGA10 are expressed throughout early anther primordia but resolve to the middle and tapetum layers during meiosis of pollen mother cells. Several lines of evidence suggest that ROXY promotion of anther development is mediated in part by TGA9 and TGA10. First, TGA9 and TGA10 expression overlaps with ROXY1/2 during anther development. Second, TGA9/10 and ROXY1/2 operate downstream of SPOROCYTELESS/NOZZLE, where they positively regulate a common set of genes that contribute to tapetal development. Third, TGA9 and TGA10 directly interact with ROXY proteins in yeast and in plant cell nuclei. These findings suggest that activation of TGA9/10 transcription factors by ROXY-mediated modification of cysteine residues promotes anther development, thus broadening our understanding of how redox-regulated TGA factors function in plants.
Highlights
ROXY1 and ROXY2 are CC-type floral glutaredoxins with redundant functions in Arabidopsis (Arabidopsis thaliana) anther development
We show here that two previously uncharacterized Arabidopsis TGA bZIP family members, TGA9 and TGA10, have overlapping functions in anther development
A similar differential block in adaxial anther lobe development is seen in roxy1 roxy2 double mutants, suggesting that TGA9 and TGA10 may be substrates of the CC-type floral glutaredoxins, ROXY1 and ROXY2
Summary
ROXY1 and ROXY2 are CC-type floral glutaredoxins with redundant functions in Arabidopsis (Arabidopsis thaliana) anther development. Histological analysis shows multiple defects in the anther dehiscence program, including abnormal stability and lignification of the middle layer and defects in septum and stomium function Compatible with these defects, TGA9 and TGA10 are expressed throughout early anther primordia but resolve to the middle and tapetum layers during meiosis of pollen mother cells. TGA9 and TGA10 directly interact with ROXY proteins in yeast and in plant cell nuclei These findings suggest that activation of TGA9/10 transcription factors by ROXY-mediated modification of cysteine residues promotes anther development, broadening our understanding of how redox-regulated TGA factors function in plants. A pair of Cys residues in the C terminus of TGA1 or TGA4 form an intermolecular disulfide bridge that is reduced upon exposure to salicylic acid (SA; Despres et al, 2003) This modification stimulates DNA binding and permits interaction with the BTB-ankryin protein NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1), a transcriptional coactivator (Despres et al, 2003; Rochon et al, 2006). Anther cell layers are specified but development of pollen mother cells and the tapetum is abnormal, leading to microspore degradation (Xing and Zachgo, 2008)
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