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

The genus 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 paren...

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Published inFrontiers in plant science Vol. 11; p. 193
Main Authors Kaga, Yuki, Yokoyama, Ryusuke, Sano, Ryosuke, Ohtani, Misato, Demura, Taku, Kuroha, Takeshi, Shinohara, Naoki, Nishitani, Kazuhiko
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 13.03.2020
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Abstract The genus 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 haustorium induction system for using rosette leaves as the host plant tissue. The 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 , we performed a transcriptome analysis using samples from the 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 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.
AbstractList The genus 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 haustorium induction system for using rosette leaves as the host plant tissue. The 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 , we performed a transcriptome analysis using samples from the 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 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.
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.
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.
Author Nishitani, Kazuhiko
Kaga, Yuki
Kuroha, Takeshi
Yokoyama, Ryusuke
Sano, Ryosuke
Ohtani, Misato
Demura, Taku
Shinohara, Naoki
AuthorAffiliation 4 Faculty of Science, Kanagawa University, Hiratsuka , Kanagawa , Japan
2 Graduate School of Science and Technology, Nara Institute of Science and Technology , Ikoma , Japan
1 Graduate School of Life Sciences, Tohoku University , Sendai , Japan
3 Graduate School of Frontier Sciences, The University of Tokyo , Kashiwa , Japan
AuthorAffiliation_xml – name: 1 Graduate School of Life Sciences, Tohoku University , Sendai , Japan
– name: 2 Graduate School of Science and Technology, Nara Institute of Science and Technology , Ikoma , Japan
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Copyright Copyright © 2020 Kaga, Yokoyama, Sano, Ohtani, Demura, Kuroha, Shinohara and Nishitani.
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Keywords haustorium development
stem parasitic plant
xylem vessel differentiation
transcriptome analysis
plant-plant interspecific interaction
Language English
License Copyright © 2020 Kaga, Yokoyama, Sano, Ohtani, Demura, Kuroha, Shinohara and Nishitani.
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Reviewed by: Takashi Ueda, National Institute for Basic Biology, Japan; Yasunori Ichihashi, RIKEN, Japan
Present address: Takeshi Kuroha, Division of Applied Genetics, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Tsukuba, Japan
This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Plant Science
Edited by: Shinichiro Sawa, Kumamoto University, Japan
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Snippet The genus is stem parasitic angiosperms that parasitize a wide range of vascular plants via de novo formation of a distinctive parasitic organ called a...
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...
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...
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StartPage 193
SubjectTerms haustorium development
Plant Science
plant-plant interspecific interaction
stem parasitic plant
transcriptome analysis
xylem vessel differentiation
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Title Interspecific Signaling Between the Parasitic Plant and the Host Plants Regulate Xylem Vessel Cell Differentiation in Haustoria of Cuscuta campestris
URI https://www.ncbi.nlm.nih.gov/pubmed/32231674
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https://doaj.org/article/3540e466f74c4bb1b28400480b230bf1
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