PERSISTENT TAPETAL CELL1Encodes a PHD-Finger Protein That Is Required for Tapetal Cell Death and Pollen Development in Rice

Hui Li,Jie Zong,Zheng Yuan,Zoe A Wilson,Wanqi Liang,Dabing Zhang,Caiyun Yang,Gema Vizcay-Barrena

doi:10.1104/pp.111.175760

Hui Li, Jie Zong + Show 6 more

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https://doi.org/10.1104/pp.111.175760

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Abstract

In higher plants, timely degradation of tapetal cells, the innermost sporophytic cells of the anther wall layer, is a prerequisite for the development of viable pollen grains. However, relatively little is known about the mechanism underlying programmed tapetal cell development and degradation. Here, we report a key regulator in monocot rice (Oryza sativa), PERSISTANT TAPETAL CELL1 (PTC1), which controls programmed tapetal development and functional pollen formation. The evolutionary significance of PTC1 was revealed by partial genetic complementation of the homologous mutation MALE STERILITY1 (MS1) in the dicot Arabidopsis (Arabidopsis thaliana). PTC1 encodes a PHD-finger (for plant homeodomain) protein, which is expressed specifically in tapetal cells and microspores during anther development in stages 8 and 9, when the wild-type tapetal cells initiate a typical apoptosis-like cell death. Even though ptc1 mutants show phenotypic similarity to ms1 in a lack of tapetal DNA fragmentation, delayed tapetal degeneration, as well as abnormal pollen wall formation and aborted microspore development, the ptc1 mutant displays a previously unreported phenotype of uncontrolled tapetal proliferation and subsequent commencement of necrosis-like tapetal death. Microarray analysis indicated that 2,417 tapetum- and microspore-expressed genes, which are principally associated with tapetal development, degeneration, and pollen wall formation, had changed expression in ptc1 anthers. Moreover, the regulatory role of PTC1 in anther development was revealed by comparison with MS1 and other rice anther developmental regulators. These findings suggest a diversified and conserved switch of PTC1/MS1 in regulating programmed male reproductive development in both dicots and monocots, which provides new insights in plant anther development.

Highlights

In higher plants, timely degradation of tapetal cells, the innermost sporophytic cells of the anther wall layer, is a prerequisite for the development of viable pollen grains
Several genes encoding putative transcription factors have been reported to be associated with tapetal function and degeneration, such as Arabidopsis (Arabidopsis thaliana) MYB33/MYB65 (Millar and Gubler, 2005), DYSFUNCTIONAL TAPETUM1 (DYT1; Zhang et al, 2006), ABORTED MICROSPORE (AMS; Sorensen et al, 2003; Xu et al, 2010), and MALE STERILITY1 (MS1; Wilson et al, 2001; Ito and Shinozaki, 2002) and rice (Oryza sativa) GAMYB (Kaneko et al, 2004; Aya et al, 2009; Liu et al, 2010), UNDEVELOPED TAPETUM1 (UDT1; Jung et al, 2005), TAPETUM DEGENERATION RETARDATION (TDR; Li et al, 2006), and MADS3 (Hu et al, 2011), their detailed functional roles in regulating tapetal Programmed cell death (PCD) during anther development are unclear
We have shown that the Arabidopsis ms1 mutant displays altered tapetal development, with a lack of normal PCD and abnormal tapetal degeneration associated with large autophagic vacuoles and mitochondrial swelling (Vizcay-Barrena and Wilson, 2006)

Summary

Introduction

Timely degradation of tapetal cells, the innermost sporophytic cells of the anther wall layer, is a prerequisite for the development of viable pollen grains. Several genes encoding putative transcription factors have been reported to be associated with tapetal function and degeneration, such as Arabidopsis (Arabidopsis thaliana) MYB33/MYB65 (Millar and Gubler, 2005), DYSFUNCTIONAL TAPETUM1 (DYT1; Zhang et al, 2006), ABORTED MICROSPORE (AMS; Sorensen et al, 2003; Xu et al, 2010), and MALE STERILITY1 (MS1; Wilson et al, 2001; Ito and Shinozaki, 2002) and rice (Oryza sativa) GAMYB (Kaneko et al, 2004; Aya et al, 2009; Liu et al, 2010), UNDEVELOPED TAPETUM1 (UDT1; Jung et al, 2005), TAPETUM DEGENERATION RETARDATION (TDR; Li et al, 2006), and MADS3 (Hu et al, 2011), their detailed functional roles in regulating tapetal PCD during anther development are unclear. GAMYB has been shown to be regulated by GA, and the gamyb tapetal cells appear swollen and have defects in PCD (Aya et al, 2009; Liu et al, 2010)

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