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The role of strigolactones in P deficiency induced transcriptional changes in tomato roots

BACKGROUND: Phosphorus (P) is an essential macronutrient for plant growth and development. Upon P shortage, plant responds with massive reprogramming of transcription, the Phosphate Starvation Response (PSR). In parallel, the production of strigolactones (SLs)—a class of plant hormones that regulate...

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Autores principales: Wang, Yanting, Duran, Hernando G. Suárez, van Haarst, Jan C., Schijlen, Elio G.W.M, Ruyter-Spira, Carolien, Medema, Marnix H., Dong, Lemeng, Bouwmeester, Harro J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8299696/
https://www.ncbi.nlm.nih.gov/pubmed/34301182
http://dx.doi.org/10.1186/s12870-021-03124-0
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author Wang, Yanting
Duran, Hernando G. Suárez
van Haarst, Jan C.
Schijlen, Elio G.W.M
Ruyter-Spira, Carolien
Medema, Marnix H.
Dong, Lemeng
Bouwmeester, Harro J.
author_facet Wang, Yanting
Duran, Hernando G. Suárez
van Haarst, Jan C.
Schijlen, Elio G.W.M
Ruyter-Spira, Carolien
Medema, Marnix H.
Dong, Lemeng
Bouwmeester, Harro J.
author_sort Wang, Yanting
collection PubMed
description BACKGROUND: Phosphorus (P) is an essential macronutrient for plant growth and development. Upon P shortage, plant responds with massive reprogramming of transcription, the Phosphate Starvation Response (PSR). In parallel, the production of strigolactones (SLs)—a class of plant hormones that regulates plant development and rhizosphere signaling molecules—increases. It is unclear, however, what the functional link is between these two processes. In this study, using tomato as a model, RNAseq was used to evaluate the time-resolved changes in gene expression in the roots upon P starvation and, using a tomato CAROTENOID CLEAVAGE DIOXYGENASES 8 (CCD8) RNAi line, what the role of SLs is in this. RESULTS: Gene ontology (GO)-term enrichment and KEGG analysis of the genes regulated by P starvation and P replenishment revealed that metabolism is an important component of the P starvation response that is aimed at P homeostasis, with large changes occurring in glyco-and galactolipid and carbohydrate metabolism, biosynthesis of secondary metabolites, including terpenoids and polyketides, glycan biosynthesis and metabolism, and amino acid metabolism. In the CCD8 RNAi line about 96% of the PSR genes was less affected than in wild-type (WT) tomato. For example, phospholipid biosynthesis was suppressed by P starvation, while the degradation of phospholipids and biosynthesis of substitute lipids such as sulfolipids and galactolipids were induced by P starvation. Around two thirds of the corresponding transcriptional changes depend on the presence of SLs. Other biosynthesis pathways are also reprogrammed under P starvation, such as phenylpropanoid and carotenoid biosynthesis, pantothenate and CoA, lysine and alkaloids, and this also partially depends on SLs. Additionally, some plant hormone biosynthetic pathways were affected by P starvation and also here, SLs are required for many of the changes (more than two thirds for Gibberellins and around one third for Abscisic acid) in the gene expression. CONCLUSIONS: Our analysis shows that SLs are not just the end product of the PSR in plants (the signals secreted by plants into the rhizosphere), but also play a major role in the regulation of the PSR (as plant hormone). SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03124-0.
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spelling pubmed-82996962021-07-28 The role of strigolactones in P deficiency induced transcriptional changes in tomato roots Wang, Yanting Duran, Hernando G. Suárez van Haarst, Jan C. Schijlen, Elio G.W.M Ruyter-Spira, Carolien Medema, Marnix H. Dong, Lemeng Bouwmeester, Harro J. BMC Plant Biol Research BACKGROUND: Phosphorus (P) is an essential macronutrient for plant growth and development. Upon P shortage, plant responds with massive reprogramming of transcription, the Phosphate Starvation Response (PSR). In parallel, the production of strigolactones (SLs)—a class of plant hormones that regulates plant development and rhizosphere signaling molecules—increases. It is unclear, however, what the functional link is between these two processes. In this study, using tomato as a model, RNAseq was used to evaluate the time-resolved changes in gene expression in the roots upon P starvation and, using a tomato CAROTENOID CLEAVAGE DIOXYGENASES 8 (CCD8) RNAi line, what the role of SLs is in this. RESULTS: Gene ontology (GO)-term enrichment and KEGG analysis of the genes regulated by P starvation and P replenishment revealed that metabolism is an important component of the P starvation response that is aimed at P homeostasis, with large changes occurring in glyco-and galactolipid and carbohydrate metabolism, biosynthesis of secondary metabolites, including terpenoids and polyketides, glycan biosynthesis and metabolism, and amino acid metabolism. In the CCD8 RNAi line about 96% of the PSR genes was less affected than in wild-type (WT) tomato. For example, phospholipid biosynthesis was suppressed by P starvation, while the degradation of phospholipids and biosynthesis of substitute lipids such as sulfolipids and galactolipids were induced by P starvation. Around two thirds of the corresponding transcriptional changes depend on the presence of SLs. Other biosynthesis pathways are also reprogrammed under P starvation, such as phenylpropanoid and carotenoid biosynthesis, pantothenate and CoA, lysine and alkaloids, and this also partially depends on SLs. Additionally, some plant hormone biosynthetic pathways were affected by P starvation and also here, SLs are required for many of the changes (more than two thirds for Gibberellins and around one third for Abscisic acid) in the gene expression. CONCLUSIONS: Our analysis shows that SLs are not just the end product of the PSR in plants (the signals secreted by plants into the rhizosphere), but also play a major role in the regulation of the PSR (as plant hormone). SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03124-0. BioMed Central 2021-07-23 /pmc/articles/PMC8299696/ /pubmed/34301182 http://dx.doi.org/10.1186/s12870-021-03124-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wang, Yanting
Duran, Hernando G. Suárez
van Haarst, Jan C.
Schijlen, Elio G.W.M
Ruyter-Spira, Carolien
Medema, Marnix H.
Dong, Lemeng
Bouwmeester, Harro J.
The role of strigolactones in P deficiency induced transcriptional changes in tomato roots
title The role of strigolactones in P deficiency induced transcriptional changes in tomato roots
title_full The role of strigolactones in P deficiency induced transcriptional changes in tomato roots
title_fullStr The role of strigolactones in P deficiency induced transcriptional changes in tomato roots
title_full_unstemmed The role of strigolactones in P deficiency induced transcriptional changes in tomato roots
title_short The role of strigolactones in P deficiency induced transcriptional changes in tomato roots
title_sort role of strigolactones in p deficiency induced transcriptional changes in tomato roots
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8299696/
https://www.ncbi.nlm.nih.gov/pubmed/34301182
http://dx.doi.org/10.1186/s12870-021-03124-0
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