Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris

The genus Cuscuta is stem parasitic angiosperms that parasitize a wide range of vascular plants via de novo formation of a distinctive parasitic organ called a haustorium. In the developing haustorium, meristematic cells, which are initiated from the stem cortical tissue, differentiate into haustori...

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Main Authors: Yuki Kaga, Ryusuke Yokoyama, Ryosuke Sano, Misato Ohtani, Taku Demura, Takeshi Kuroha, Naoki Shinohara, Kazuhiko Nishitani
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00193/full
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author Yuki Kaga
Ryusuke Yokoyama
Ryosuke Sano
Misato Ohtani
Misato Ohtani
Taku Demura
Takeshi Kuroha
Naoki Shinohara
Kazuhiko Nishitani
Kazuhiko Nishitani
author_facet Yuki Kaga
Ryusuke Yokoyama
Ryosuke Sano
Misato Ohtani
Misato Ohtani
Taku Demura
Takeshi Kuroha
Naoki Shinohara
Kazuhiko Nishitani
Kazuhiko Nishitani
author_sort Yuki Kaga
collection DOAJ
description The genus Cuscuta is stem parasitic angiosperms that parasitize a wide range of vascular plants via de novo formation of a distinctive parasitic organ called a haustorium. In the developing haustorium, meristematic cells, which are initiated from the stem cortical tissue, differentiate into haustorial parenchyma cells, which elongate, penetrate into the host tissues, and finally connect with the host vasculature. This interspecific vasculature connection allows the parasite to uptake water and nutrients from the host plant. Although histological aspects of haustorium development have been studied extensively, the molecular mechanisms underlying vasculature development and the interspecific connection with the host vasculature remain largely unknown. To gain insights into the interspecific cell-to-cell interactions involved in haustorium development, we established an in vitro haustorium induction system for Cuscuta campestris using Arabidopsis thaliana rosette leaves as the host plant tissue. The in vitro induction system was used to show that interaction with host tissue was required for the differentiation of parasite haustorial cells into xylem vessel cells. To further characterize the molecular events occurring during host-dependent xylem vessel cell differentiation in C. campestris, we performed a transcriptome analysis using samples from the in vitro induction system. The results showed that orthologs of genes involved in development and proliferation of vascular stem cells were up-regulated even in the absence of host tissue, whereas orthologs of genes required for xylem vessel cell differentiation were up-regulated only after some haustorial cells had elongated and contacted the host xylem. Consistent results were obtained by another transcriptome analysis of the haustorium development in C. campestris undergoing parasitization of an intact host plant. These findings suggest the involvement of host-derived signals in the regulation of non-autonomous xylem vessel differentiation and suggest that its connection to the host xylem during the haustorium development activates a set of key genes for differentiation into xylem vessel cells.
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spelling doaj.art-3540e466f74c4bb1b28400480b230bf12022-12-22T01:18:47ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-03-011110.3389/fpls.2020.00193524693Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestrisYuki Kaga0Ryusuke Yokoyama1Ryosuke Sano2Misato Ohtani3Misato Ohtani4Taku Demura5Takeshi Kuroha6Naoki Shinohara7Kazuhiko Nishitani8Kazuhiko Nishitani9Graduate School of Life Sciences, Tohoku University, Sendai, JapanGraduate School of Life Sciences, Tohoku University, Sendai, JapanGraduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, JapanGraduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, JapanGraduate School of Frontier Sciences, The University of Tokyo, Kashiwa, JapanGraduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, JapanGraduate School of Life Sciences, Tohoku University, Sendai, JapanFaculty of Science, Kanagawa University, Hiratsuka, Kanagawa, JapanGraduate School of Life Sciences, Tohoku University, Sendai, JapanFaculty of Science, Kanagawa University, Hiratsuka, Kanagawa, JapanThe genus Cuscuta is stem parasitic angiosperms that parasitize a wide range of vascular plants via de novo formation of a distinctive parasitic organ called a haustorium. In the developing haustorium, meristematic cells, which are initiated from the stem cortical tissue, differentiate into haustorial parenchyma cells, which elongate, penetrate into the host tissues, and finally connect with the host vasculature. This interspecific vasculature connection allows the parasite to uptake water and nutrients from the host plant. Although histological aspects of haustorium development have been studied extensively, the molecular mechanisms underlying vasculature development and the interspecific connection with the host vasculature remain largely unknown. To gain insights into the interspecific cell-to-cell interactions involved in haustorium development, we established an in vitro haustorium induction system for Cuscuta campestris using Arabidopsis thaliana rosette leaves as the host plant tissue. The in vitro induction system was used to show that interaction with host tissue was required for the differentiation of parasite haustorial cells into xylem vessel cells. To further characterize the molecular events occurring during host-dependent xylem vessel cell differentiation in C. campestris, we performed a transcriptome analysis using samples from the in vitro induction system. The results showed that orthologs of genes involved in development and proliferation of vascular stem cells were up-regulated even in the absence of host tissue, whereas orthologs of genes required for xylem vessel cell differentiation were up-regulated only after some haustorial cells had elongated and contacted the host xylem. Consistent results were obtained by another transcriptome analysis of the haustorium development in C. campestris undergoing parasitization of an intact host plant. These findings suggest the involvement of host-derived signals in the regulation of non-autonomous xylem vessel differentiation and suggest that its connection to the host xylem during the haustorium development activates a set of key genes for differentiation into xylem vessel cells.https://www.frontiersin.org/article/10.3389/fpls.2020.00193/fullstem parasitic plantplant-plant interspecific interactionhaustorium developmentxylem vessel differentiationtranscriptome analysis
spellingShingle Yuki Kaga
Ryusuke Yokoyama
Ryosuke Sano
Misato Ohtani
Misato Ohtani
Taku Demura
Takeshi Kuroha
Naoki Shinohara
Kazuhiko Nishitani
Kazuhiko Nishitani
Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
Frontiers in Plant Science
stem parasitic plant
plant-plant interspecific interaction
haustorium development
xylem vessel differentiation
transcriptome analysis
title Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
title_full Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
title_fullStr Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
title_full_unstemmed Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
title_short Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
title_sort interspecific signaling between the parasitic plant and the host plants regulate xylem vessel cell differentiation in haustoria of cuscuta campestris
topic stem parasitic plant
plant-plant interspecific interaction
haustorium development
xylem vessel differentiation
transcriptome analysis
url https://www.frontiersin.org/article/10.3389/fpls.2020.00193/full
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