Proline synthesis in developing microspores is required for pollen development and fertility

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2018
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Mattioli, Roberto
Biancucci, Marco
El Shall, Amira
Mosca, Luciana
Costantino, Paolo
Trovato, Maurizio
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BMC plant biology. 2018, 18(1), 356. eISSN 1471-2229. Available under: doi: 10.1186/s12870-018-1571-3
Zusammenfassung

Background:
In many plants, the amino acid proline is strongly accumulated in pollen and disruption of proline synthesis caused abortion of microspore development in Arabidopsis. So far, it was unclear whether local biosynthesis or transport of proline determines the success of fertile pollen development.

Results:
We analyzed the expression pattern of the proline biosynthetic genes PYRROLINE-5-CARBOXYLATE SYNTHETASE 1 & 2 (P5CS1 & 2) in Arabidopsis anthers and both isoforms were strongly expressed in developing microspores and pollen grains but only inconsistently in surrounding sporophytic tissues. We introduced in a p5cs1/p5cs1 p5cs2/P5CS2 mutant background an additional copy of P5CS2 under the control of the Cauliflower Mosaic Virus (CaMV) 35S promoter, the tapetum-specific LIPID TRANSFER PROTEIN 12 (Ltp12) promoter or the pollen-specific At5g17340 promoter to determine in which site proline biosynthesis can restore the fertility of proline-deficient microspores. The specificity of these promoters was confirmed by β-glucuronidase (GUS) analysis, and by direct proline measurement in pollen grains and stage-9/10 anthers. Expression of P5CS2 under control of the At5g17340 promoter fully rescued proline content and normal morphology and fertility of mutant pollen. In contrast, expression of P5CS2 driven by either the Ltp12 or CaMV35S promoter caused only partial restoration of pollen development with little effect on pollen fertility.

Conclusions:
Overall, our results indicate that proline transport is not able to fulfill the demand of the cells of the male germ line. Pollen development and fertility depend on local proline biosynthesis during late stages of microspore development and in mature pollen grains.

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570 Biowissenschaften, Biologie
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Proline biosynthesis, Pollen development, Tissue specificity, Anthers, Arabidopsis
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ISO 690MATTIOLI, Roberto, Marco BIANCUCCI, Amira EL SHALL, Luciana MOSCA, Paolo COSTANTINO, Dietmar FUNCK, Maurizio TROVATO, 2018. Proline synthesis in developing microspores is required for pollen development and fertility. In: BMC plant biology. 2018, 18(1), 356. eISSN 1471-2229. Available under: doi: 10.1186/s12870-018-1571-3
BibTex
@article{Mattioli2018-12-17Proli-44616,
  year={2018},
  doi={10.1186/s12870-018-1571-3},
  title={Proline synthesis in developing microspores is required for pollen development and fertility},
  number={1},
  volume={18},
  journal={BMC plant biology},
  author={Mattioli, Roberto and Biancucci, Marco and El Shall, Amira and Mosca, Luciana and Costantino, Paolo and Funck, Dietmar and Trovato, Maurizio},
  note={Article Number: 356}
}
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    <dcterms:abstract xml:lang="eng">Background:&lt;br /&gt;In many plants, the amino acid proline is strongly accumulated in pollen and disruption of proline synthesis caused abortion of microspore development in Arabidopsis. So far, it was unclear whether local biosynthesis or transport of proline determines the success of fertile pollen development.&lt;br /&gt;&lt;br /&gt;Results:&lt;br /&gt;We analyzed the expression pattern of the proline biosynthetic genes PYRROLINE-5-CARBOXYLATE SYNTHETASE 1 &amp; 2 (P5CS1 &amp; 2) in Arabidopsis anthers and both isoforms were strongly expressed in developing microspores and pollen grains but only inconsistently in surrounding sporophytic tissues. We introduced in a p5cs1/p5cs1 p5cs2/P5CS2 mutant background an additional copy of P5CS2 under the control of the Cauliflower Mosaic Virus (CaMV) 35S promoter, the tapetum-specific LIPID TRANSFER PROTEIN 12 (Ltp12) promoter or the pollen-specific At5g17340 promoter to determine in which site proline biosynthesis can restore the fertility of proline-deficient microspores. The specificity of these promoters was confirmed by β-glucuronidase (GUS) analysis, and by direct proline measurement in pollen grains and stage-9/10 anthers. Expression of P5CS2 under control of the At5g17340 promoter fully rescued proline content and normal morphology and fertility of mutant pollen. In contrast, expression of P5CS2 driven by either the Ltp12 or CaMV35S promoter caused only partial restoration of pollen development with little effect on pollen fertility.&lt;br /&gt;&lt;br /&gt;Conclusions:&lt;br /&gt;Overall, our results indicate that proline transport is not able to fulfill the demand of the cells of the male germ line. Pollen development and fertility depend on local proline biosynthesis during late stages of microspore development and in mature pollen grains.</dcterms:abstract>
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