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

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

Research output: Contribution to journalArticle

123 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)2225-2246
Number of pages22
JournalPlant Cell
Volume23
Issue number6
DOIs
StatePublished - Jan 1 2011

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Acyl Carrier Protein
acyl carrier protein
microspores
Pollen
anthers
Oxidoreductases
Fatty Alcohols
pollen
rice
fatty alcohols
Magnoliopsida
Liliopsida
biosynthesis
fatty acids
cutin
mutants
Plastids
exine
epicuticular wax
Waxes

All Science Journal Classification (ASJC) codes

  • Plant Science
  • Cell Biology

Cite this

Shi, Jing ; Tan, Hexin ; Yu, Xiao Hong ; Liu, Yuanyun ; Liang, Wanqi ; Ranathunge, Kosala ; Franke, Rochus Benni ; Schreiber, Lukas ; Wang, Yujiong ; Kai, Guoying ; Shanklin, John ; Ma, Hong ; Zhang, Dabing. / Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. In: Plant Cell. 2011 ; Vol. 23, No. 6. pp. 2225-2246.
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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.",
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Shi, J, Tan, H, Yu, XH, Liu, Y, Liang, W, Ranathunge, K, Franke, RB, Schreiber, L, Wang, Y, Kai, G, Shanklin, J, Ma, H & Zhang, D 2011, 'Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase', Plant Cell, vol. 23, no. 6, pp. 2225-2246. https://doi.org/10.1105/tpc.111.087528

Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. / Shi, Jing; Tan, Hexin; Yu, Xiao Hong; Liu, Yuanyun; Liang, Wanqi; Ranathunge, Kosala; Franke, Rochus Benni; Schreiber, Lukas; Wang, Yujiong; Kai, Guoying; Shanklin, John; Ma, Hong; Zhang, Dabing.

In: Plant Cell, Vol. 23, No. 6, 01.01.2011, p. 2225-2246.

Research output: Contribution to journalArticle

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AU - Shi, Jing

AU - Tan, Hexin

AU - Yu, Xiao Hong

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AU - Liang, Wanqi

AU - Ranathunge, Kosala

AU - Franke, Rochus Benni

AU - Schreiber, Lukas

AU - Wang, Yujiong

AU - Kai, Guoying

AU - Shanklin, John

AU - Ma, Hong

AU - Zhang, Dabing

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N2 - 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.

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