COLLAPSED ABNORMAL POLLEN1Gene Encoding the Arabinokinase-Like Protein Is Involved in Pollen Development in Rice

Kenji Ueda,Fumiaki Yoshimura,Hirohiko Hirochika,Ken-Ichi Nonomura,Akio Miyao,Hiroetsu Wabiko

doi:10.1104/pp.113.216523

Abstract

We isolated a pollen-defective mutant, collapsed abnormal pollen1 (cap1), from Tos17 insertional mutant lines of rice (Oryza sativa). The cap1 heterozygous plant produced equal numbers of normal and collapsed abnormal grains. The abnormal pollen grains lacked almost all cytoplasmic materials, nuclei, and intine cell walls and did not germinate. Genetic analysis of crosses revealed that the cap1 mutation did not affect female reproduction or vegetative growth. CAP1 encodes a protein consisting of 996 amino acids that showed high similarity to Arabidopsis (Arabidopsis thaliana) l-arabinokinase, which catalyzes the conversion of l-arabinose to l-arabinose 1-phosphate. A wild-type genomic DNA segment containing CAP1 restored mutants to normal pollen grains. During rice pollen development, CAP1 was preferentially expressed in anthers at the bicellular pollen stage, and the effects of the cap1 mutation were mainly detected at this stage. Based on the metabolic pathway of l-arabinose, cap1 pollen phenotype may have been caused by toxic accumulation of l-arabinose or by inhibition of cell wall metabolism due to the lack of UDP-l-arabinose derived from l-arabinose 1-phosphate. The expression pattern of CAP1 was very similar to that of another Arabidopsis homolog that showed 71% amino acid identity with CAP1. Our results suggested that CAP1 and related genes are critical for pollen development in both monocotyledonous and dicotyledonous plants.

Highlights

We isolated a pollen-defective mutant, collapsed abnormal pollen1, from Tos17 insertional mutant lines of rice (Oryza sativa)
Mutant analyses of defective tapetums have revealed several genes critical for pollen development, such as the gibberellin-regulated R2R3 MYB transcription factor GAMYB; the C2-GRAM domain protein gene ORYZA SATIVA NO POLLEN; UNDEVELOPED TAPETUM1, which encodes a basic helix-loop-helix transcription factor; WAX-DEFICIENT ANTHER1, encoding an enzyme involved in the synthesis of very-long-chain fatty acids; basic helix-loophelix protein genes TAPETUM DEGENERATION RETARDATION and ETERNAL TAPETUM1 (EAT1); UDP GLC PYROPHOSPHORYLASE1 (UGP1); the lipid transfer protein gene named OsC6; the R2R3 MYB transcription factor CARBON STARVED ANTHER (CSA); a cytochrome P450 family gene, CYP704B2; a C-class MADS box gene, MADS3; APOPTOSIS INHIBITOR5 (API5); and MICROSPORE AND TAPETUM REGULATOR1
The AtARA2 gene was preferentially expressed in pollen and at especially high levels during the bicellular stage (Supplemental Fig. S5). These results suggested that AtARA2 in Arabidopsis is an ortholog of COLLAPSED ABNORMAL POLLEN1 (CAP1) and that the putative arabinokinase is important for pollen development in both monocotyledonous and dicotyledonous plants

Summary

Introduction

We isolated a pollen-defective mutant, collapsed abnormal pollen (cap1), from Tos insertional mutant lines of rice (Oryza sativa). Mutant analyses of defective tapetums have revealed several genes critical for pollen development, such as the gibberellin-regulated R2R3 MYB transcription factor GAMYB; the C2-GRAM domain protein gene ORYZA SATIVA NO POLLEN; UNDEVELOPED TAPETUM1, which encodes a basic helix-loop-helix transcription factor; WAX-DEFICIENT ANTHER1, encoding an enzyme involved in the synthesis of very-long-chain fatty acids; basic helix-loophelix protein genes TAPETUM DEGENERATION RETARDATION and ETERNAL TAPETUM1 (EAT1); UDP GLC PYROPHOSPHORYLASE1 (UGP1); the lipid transfer protein gene named OsC6; the R2R3 MYB transcription factor CARBON STARVED ANTHER (CSA); a cytochrome P450 family gene, CYP704B2; a C-class MADS box gene, MADS3; APOPTOSIS INHIBITOR5 (API5); and MICROSPORE AND TAPETUM REGULATOR1 In these mutants, cells within anthers began to degenerate at the meiosis or microspore stages, eventually resulting in no pollen or complete pollen collapse (Kaneko et al, 2004; Jiang et al, 2005; Jung et al, 2005, 2006; Li et al, 2006, 2010a, 2011; Chen et al, 2007; Chhun et al, 2007; Aya et al, 2009; Zhang et al, 2010a, 2010b, 2013; Hu et al, 2011; Tan et al, 2012; Niu et al, 2013)

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