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Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections

Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396–GRF1/3 module is a master regulator of syncytium developme...

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Autores principales: Noon, Jason B, Hewezi, Tarek, Baum, Thomas J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6411377/
https://www.ncbi.nlm.nih.gov/pubmed/30715445
http://dx.doi.org/10.1093/jxb/erz022
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author Noon, Jason B
Hewezi, Tarek
Baum, Thomas J
author_facet Noon, Jason B
Hewezi, Tarek
Baum, Thomas J
author_sort Noon, Jason B
collection PubMed
description Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396–GRF1/3 module is a master regulator of syncytium development in model cyst nematode H. schachtii infection of Arabidopsis. Here, we investigated whether this regulatory system operates similarly in soybean roots and is likewise important for H. glycines infection. We found that a network involving nine MIR396 and 23 GRF genes is important for normal development of soybean roots and that GRF function is specified in the root apical meristem by miR396. All MIR396 genes are down-regulated in the syncytium during its formation phase while, specifically, 11 different GRF genes are up-regulated. The switch to the syncytium maintenance phase coincides with up-regulation of MIR396 and down-regulation of the 11 GRF genes specifically via post-transcriptional regulation by miR396. Furthermore, interference with the miR396–GRF6/8–13/15–17/19 regulatory network, through either overexpression or knockdown experiments, does not affect the number of H. glycines juveniles that enter the vascular cylinder to initiate syncytia, but specifically inhibits efficient H. glycines development to adult females. Therefore, homeostasis in the miR396–GRF6/8–13/15–17/19 regulatory network is essential for productive H. glycines infections.
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spelling pubmed-64113772019-03-15 Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections Noon, Jason B Hewezi, Tarek Baum, Thomas J J Exp Bot Research Papers Heterodera glycines, the soybean cyst nematode, penetrates soybean roots and migrates to the vascular cylinder where it forms a feeding site called the syncytium. MiRNA396 (miR396) targets growth-regulating factor (GRF) genes, and the miR396–GRF1/3 module is a master regulator of syncytium development in model cyst nematode H. schachtii infection of Arabidopsis. Here, we investigated whether this regulatory system operates similarly in soybean roots and is likewise important for H. glycines infection. We found that a network involving nine MIR396 and 23 GRF genes is important for normal development of soybean roots and that GRF function is specified in the root apical meristem by miR396. All MIR396 genes are down-regulated in the syncytium during its formation phase while, specifically, 11 different GRF genes are up-regulated. The switch to the syncytium maintenance phase coincides with up-regulation of MIR396 and down-regulation of the 11 GRF genes specifically via post-transcriptional regulation by miR396. Furthermore, interference with the miR396–GRF6/8–13/15–17/19 regulatory network, through either overexpression or knockdown experiments, does not affect the number of H. glycines juveniles that enter the vascular cylinder to initiate syncytia, but specifically inhibits efficient H. glycines development to adult females. Therefore, homeostasis in the miR396–GRF6/8–13/15–17/19 regulatory network is essential for productive H. glycines infections. Oxford University Press 2019-02-15 2019-01-30 /pmc/articles/PMC6411377/ /pubmed/30715445 http://dx.doi.org/10.1093/jxb/erz022 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Papers
Noon, Jason B
Hewezi, Tarek
Baum, Thomas J
Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections
title Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections
title_full Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections
title_fullStr Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections
title_full_unstemmed Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections
title_short Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections
title_sort homeostasis in the soybean mirna396–grf network is essential for productive soybean cyst nematode infections
topic Research Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6411377/
https://www.ncbi.nlm.nih.gov/pubmed/30715445
http://dx.doi.org/10.1093/jxb/erz022
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