Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>

The pentose phosphate pathway (PPP) plays an important role in plant growth and development, and plant responses to biotic and abiotic stresses. Yet, whether the PPP regulates plant defenses against herbivorous insects remains unclear. In this study, we cloned a rice cytosolic 6-phosphogluconate deh...

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Main Authors: Lin Chen, Peng Kuai, Miaofen Ye, Shuxing Zhou, Jing Lu, Yonggen Lou
Format: Article
Language:English
Published: MDPI AG 2020-11-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/9/11/1529
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author Lin Chen
Peng Kuai
Miaofen Ye
Shuxing Zhou
Jing Lu
Yonggen Lou
author_facet Lin Chen
Peng Kuai
Miaofen Ye
Shuxing Zhou
Jing Lu
Yonggen Lou
author_sort Lin Chen
collection DOAJ
description The pentose phosphate pathway (PPP) plays an important role in plant growth and development, and plant responses to biotic and abiotic stresses. Yet, whether the PPP regulates plant defenses against herbivorous insects remains unclear. In this study, we cloned a rice cytosolic 6-phosphogluconate dehydrogenase gene, <i>Os6PGDH1</i>, which encodes the key enzyme catalyzing the third step in the reaction involving the oxidative phase of the PPP, and explored its role in rice defenses induced by brown planthopper (BPH) <i>Nilaparvata lugens</i>. Levels of <i>Os6PGDH1</i> transcripts were detected in all five examined tissues, with the highest in outer leaf sheaths and lowest in inner leaf sheaths. <i>Os6PGDH1</i> expression was strongly induced by mechanical wounding, infestation of gravid BPH females, and jasmonic acid (JA) treatment. Overexpressing <i>Os6PGDH1</i> (oe6PGDH) decreased the height of rice plants and the mass of the aboveground part of plants, but slightly increased the length of plant roots. In addition, the overexpression of <i>Os6PGDH1</i> enhanced levels of BPH-induced JA, jasmonoyl-isoleucine (JA-Ile), and H<sub>2</sub>O<sub>2</sub>, but decreased BPH-induced levels of ethylene. Bioassays revealed that gravid BPH females preferred to feed and lay eggs on wild-type (WT) plants over oe6PGDH plants; moreover, the hatching rate of BPH eggs raised on oe6PGDH plants and the fecundity of BPH females fed on these were significantly lower than the eggs and the females raised and fed on WT plants. Taken together, these results indicate that <i>Os6PGDH1</i> plays a pivotal role not only in rice growth but also in the resistance of rice to BPH by modulating JA, ethylene, and H<sub>2</sub>O<sub>2</sub> pathways.
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spelling doaj.art-b1c4ad3a6738433a9ba7ebffeff2cd7a2023-11-20T20:25:21ZengMDPI AGPlants2223-77472020-11-01911152910.3390/plants9111529Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>Lin Chen0Peng Kuai1Miaofen Ye2Shuxing Zhou3Jing Lu4Yonggen Lou5State Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, ChinaState Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, ChinaState Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, ChinaState Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, ChinaState Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, ChinaState Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, ChinaThe pentose phosphate pathway (PPP) plays an important role in plant growth and development, and plant responses to biotic and abiotic stresses. Yet, whether the PPP regulates plant defenses against herbivorous insects remains unclear. In this study, we cloned a rice cytosolic 6-phosphogluconate dehydrogenase gene, <i>Os6PGDH1</i>, which encodes the key enzyme catalyzing the third step in the reaction involving the oxidative phase of the PPP, and explored its role in rice defenses induced by brown planthopper (BPH) <i>Nilaparvata lugens</i>. Levels of <i>Os6PGDH1</i> transcripts were detected in all five examined tissues, with the highest in outer leaf sheaths and lowest in inner leaf sheaths. <i>Os6PGDH1</i> expression was strongly induced by mechanical wounding, infestation of gravid BPH females, and jasmonic acid (JA) treatment. Overexpressing <i>Os6PGDH1</i> (oe6PGDH) decreased the height of rice plants and the mass of the aboveground part of plants, but slightly increased the length of plant roots. In addition, the overexpression of <i>Os6PGDH1</i> enhanced levels of BPH-induced JA, jasmonoyl-isoleucine (JA-Ile), and H<sub>2</sub>O<sub>2</sub>, but decreased BPH-induced levels of ethylene. Bioassays revealed that gravid BPH females preferred to feed and lay eggs on wild-type (WT) plants over oe6PGDH plants; moreover, the hatching rate of BPH eggs raised on oe6PGDH plants and the fecundity of BPH females fed on these were significantly lower than the eggs and the females raised and fed on WT plants. Taken together, these results indicate that <i>Os6PGDH1</i> plays a pivotal role not only in rice growth but also in the resistance of rice to BPH by modulating JA, ethylene, and H<sub>2</sub>O<sub>2</sub> pathways.https://www.mdpi.com/2223-7747/9/11/1529rice<i>6-phosphogluconate dehydrogenase</i>herbivore-induced plant defenses<i>Nilaparvata lugens</i>
spellingShingle Lin Chen
Peng Kuai
Miaofen Ye
Shuxing Zhou
Jing Lu
Yonggen Lou
Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>
Plants
rice
<i>6-phosphogluconate dehydrogenase</i>
herbivore-induced plant defenses
<i>Nilaparvata lugens</i>
title Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>
title_full Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>
title_fullStr Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>
title_full_unstemmed Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>
title_short Overexpression of a Cytosolic 6-Phosphogluconate Dehydrogenase Gene Enhances the Resistance of Rice to <i>Nilaparvata lugens</i>
title_sort overexpression of a cytosolic 6 phosphogluconate dehydrogenase gene enhances the resistance of rice to i nilaparvata lugens i
topic rice
<i>6-phosphogluconate dehydrogenase</i>
herbivore-induced plant defenses
<i>Nilaparvata lugens</i>
url https://www.mdpi.com/2223-7747/9/11/1529
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