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Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages

Parasitic weeds cause billions of dollars in agricultural losses each year worldwide. Cuscuta campestris (C. campestris), one of the most widespread and destructive parasitic plants in the United States, severely reduces yield in tomato plants. Reducing the spread of parasitic weeds requires underst...

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Autores principales: Jhu, Min-Yao, Farhi, Moran, Wang, Li, Zumstein, Kristina, Sinha, Neelima R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8866705/
https://www.ncbi.nlm.nih.gov/pubmed/35222447
http://dx.doi.org/10.3389/fpls.2021.764843
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author Jhu, Min-Yao
Farhi, Moran
Wang, Li
Zumstein, Kristina
Sinha, Neelima R.
author_facet Jhu, Min-Yao
Farhi, Moran
Wang, Li
Zumstein, Kristina
Sinha, Neelima R.
author_sort Jhu, Min-Yao
collection PubMed
description Parasitic weeds cause billions of dollars in agricultural losses each year worldwide. Cuscuta campestris (C. campestris), one of the most widespread and destructive parasitic plants in the United States, severely reduces yield in tomato plants. Reducing the spread of parasitic weeds requires understanding the interaction between parasites and hosts. Several studies have identified factors needed for parasitic plant germination and haustorium induction, and genes involved in host defense responses. However, knowledge of the mechanisms underlying the interactions between host and parasitic plants, specifically at the interface between the two organisms, is relatively limited. A detailed investigation of the crosstalk between the host and parasite at the tissue-specific level would enable development of effective parasite control strategies. To focus on the haustorial interface, we used laser-capture microdissection (LCM) with RNA-seq on early, intermediate and mature haustorial stages. In addition, the tomato host tissue that immediately surround the haustoria was collected to obtain tissue- resolution RNA-Seq profiles for C. campestris and tomato at the parasitism interface. After conducting RNA-Seq analysis and constructing gene coexpression networks (GCNs), we identified CcHB7, CcPMEI, and CcERF1 as putative key regulators involved in C. campestris haustorium organogenesis, and three potential regulators, SlPR1, SlCuRe1-like, and SlNLR, in tomatoes that are involved in perceiving signals from the parasite. We used host-induced gene silencing (HIGS) transgenic tomatoes to knock-down the candidate genes in C. campestris and produced CRISPR transgenic tomatoes to knock out candidate genes in tomatoes. The interactions of C. campestris with these transgenic lines were tested and compared with that in wild-type tomatoes. The results of this study reveal the tissue-resolution gene regulatory mechanisms at the parasitic plant-host interface and provide the potential of developing a parasite-resistant system in tomatoes.
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spelling pubmed-88667052022-02-25 Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages Jhu, Min-Yao Farhi, Moran Wang, Li Zumstein, Kristina Sinha, Neelima R. Front Plant Sci Plant Science Parasitic weeds cause billions of dollars in agricultural losses each year worldwide. Cuscuta campestris (C. campestris), one of the most widespread and destructive parasitic plants in the United States, severely reduces yield in tomato plants. Reducing the spread of parasitic weeds requires understanding the interaction between parasites and hosts. Several studies have identified factors needed for parasitic plant germination and haustorium induction, and genes involved in host defense responses. However, knowledge of the mechanisms underlying the interactions between host and parasitic plants, specifically at the interface between the two organisms, is relatively limited. A detailed investigation of the crosstalk between the host and parasite at the tissue-specific level would enable development of effective parasite control strategies. To focus on the haustorial interface, we used laser-capture microdissection (LCM) with RNA-seq on early, intermediate and mature haustorial stages. In addition, the tomato host tissue that immediately surround the haustoria was collected to obtain tissue- resolution RNA-Seq profiles for C. campestris and tomato at the parasitism interface. After conducting RNA-Seq analysis and constructing gene coexpression networks (GCNs), we identified CcHB7, CcPMEI, and CcERF1 as putative key regulators involved in C. campestris haustorium organogenesis, and three potential regulators, SlPR1, SlCuRe1-like, and SlNLR, in tomatoes that are involved in perceiving signals from the parasite. We used host-induced gene silencing (HIGS) transgenic tomatoes to knock-down the candidate genes in C. campestris and produced CRISPR transgenic tomatoes to knock out candidate genes in tomatoes. The interactions of C. campestris with these transgenic lines were tested and compared with that in wild-type tomatoes. The results of this study reveal the tissue-resolution gene regulatory mechanisms at the parasitic plant-host interface and provide the potential of developing a parasite-resistant system in tomatoes. Frontiers Media S.A. 2022-02-10 /pmc/articles/PMC8866705/ /pubmed/35222447 http://dx.doi.org/10.3389/fpls.2021.764843 Text en Copyright © 2022 Jhu, Farhi, Wang, Zumstein and Sinha. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Jhu, Min-Yao
Farhi, Moran
Wang, Li
Zumstein, Kristina
Sinha, Neelima R.
Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages
title Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages
title_full Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages
title_fullStr Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages
title_full_unstemmed Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages
title_short Investigating Host and Parasitic Plant Interaction by Tissue-Specific Gene Analyses on Tomato and Cuscuta campestris Interface at Three Haustorial Developmental Stages
title_sort investigating host and parasitic plant interaction by tissue-specific gene analyses on tomato and cuscuta campestris interface at three haustorial developmental stages
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8866705/
https://www.ncbi.nlm.nih.gov/pubmed/35222447
http://dx.doi.org/10.3389/fpls.2021.764843
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