Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase.

Jing Shi,Guoying Kai,Rochus Benni Franke,Hexin Tan,Yuanyun Liu,Yujiong Wang,Xiao-Hong Yu,Lukas Schreiber,Kosala Ranathunge,Dabing Zhang,Hong Ma,John Shanklin,Wanqi Liang

doi:10.1105/tpc.111.087528

Abstract

Aliphatic alcohols naturally exist in many organisms as important cellular components; however, their roles in extracellular polymer biosynthesis are poorly defined. We report here the isolation and characterization of a rice (Oryza sativa) male-sterile mutant, defective pollen wall (dpw), which displays defective anther development and degenerated pollen grains with an irregular exine. Chemical analysis revealed that dpw anthers had a dramatic reduction in cutin monomers and an altered composition of cuticular wax, as well as soluble fatty acids and alcohols. Using map-based cloning, we identified the DPW gene, which is expressed in both tapetal cells and microspores during anther development. Biochemical analysis of the recombinant DPW enzyme shows that it is a novel fatty acid reductase that produces 1-hexadecanol and exhibits >270-fold higher specificity for palmiltoyl-acyl carrier protein than for C16:0 CoA substrates. DPW was predominantly targeted to plastids mediated by its N-terminal transit peptide. Moreover, we demonstrate that the monocot DPW from rice complements the dicot Arabidopsis thaliana male sterile2 (ms2) mutant and is the probable ortholog of MS2. These data suggest that DPWs participate in a conserved step in primary fatty alcohol synthesis for anther cuticle and pollen sporopollenin biosynthesis in monocots and dicots.

Highlights

Fatty alcohols naturally exist in plants, animals, and algae in free forms, but more frequently in esterified or etherified forms
To identify rice genes that are important for normal anther and pollen development, we used 60Co g-ray radiation to generate a rice mutant library in the 9522 background, which is a cultivar of O. sativa ssp japonica (Liu et al, 2005; Chen et al, 2006; Li et al, 2006; Wang et al, 2006)
Vegetative and floral development seemed to be normal in the dpw mutant plant (Figures 1A to 1C); compared with the wild type, the mutant anthers were smaller (Figures 1D and 1E) and lacked normal mature pollen grains (Figures 1F and 1G)

Summary

Introduction

Fatty alcohols naturally exist in plants, animals, and algae in free forms (the component of cuticular lipids), but more frequently in esterified (wax esters) or etherified forms (glyceryl ethers). Fatty alcohols are important cellular components, including the fatty constituents of plant cuticle, insect surface coatings, animal skin, and others (Kunst and Samuels, 2003). During pollen development in flowering plants, fatty alcohols and their derivatives are major components of the anther cuticle and pollen wall, which are rich in lipids (Ahlers et al, 1999; Meuter-Gerhards et al, 1999; Jung et al, 2006). The pollen develops a protective wall, which has two layers, the outer exine and the inner intine.

Methods

Results

Conclusion