Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>

<i>Cuscuta</i> spp. are obligate parasites that connect to host vascular tissue using a haustorium. In addition to water, nutrients, and metabolites, a large number of mRNAs are bidirectionally exchanged between <i>Cuscuta</i> spp. and their hosts. This trans-specific movemen...

Full description

Bibliographic Details
Main Authors: So-Yon Park, Kohki Shimizu, Jocelyn Brown, Koh Aoki, James H. Westwood
Format: Article
Language:English
Published: MDPI AG 2021-12-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/11/1/93
_version_ 1797497907081904128
author So-Yon Park
Kohki Shimizu
Jocelyn Brown
Koh Aoki
James H. Westwood
author_facet So-Yon Park
Kohki Shimizu
Jocelyn Brown
Koh Aoki
James H. Westwood
author_sort So-Yon Park
collection DOAJ
description <i>Cuscuta</i> spp. are obligate parasites that connect to host vascular tissue using a haustorium. In addition to water, nutrients, and metabolites, a large number of mRNAs are bidirectionally exchanged between <i>Cuscuta</i> spp. and their hosts. This trans-specific movement of mRNAs raises questions about whether these molecules function in the recipient species. To address the possibility that mobile mRNAs are ultimately translated, we built upon recent studies that demonstrate a role for transfer RNA (tRNA)-like structures (TLSs) in enhancing mRNA systemic movement. <i>C. campestris</i> was grown on <i>Arabidopsis</i> that expressed a β-glucuronidase (<i>GUS</i>) reporter transgene either alone or in <i>GUS-tRNA</i> fusions. Histochemical staining revealed localization in tissue of <i>C. campestris</i> grown on <i>Arabidopsis</i> with <i>GUS-tRNA</i> fusions, but not in <i>C. campestris</i> grown on <i>Arabidopsis</i> with <i>GUS</i> alone. This corresponded with detection of <i>GUS</i> transcripts in <i>Cuscuta</i> on <i>Arabidopsis</i> with <i>GUS-tRNA</i>, but not in <i>C. campestris</i> on <i>Arabidopsis</i> with <i>GUS</i> alone. Similar results were obtained with <i>Arabidopsis</i> host plants expressing the same constructs containing an endoplasmic reticulum localization signal. In <i>C. campestris</i>, GUS activity was localized in the companion cells or phloem parenchyma cells adjacent to sieve tubes. We conclude that host-derived <i>GUS</i> mRNAs are translated in <i>C. campestris</i> and that the TLS fusion enhances RNA mobility in the host-parasite interactions.
first_indexed 2024-03-10T03:25:51Z
format Article
id doaj.art-33eefdb020834c0ba480dadd941c7824
institution Directory Open Access Journal
issn 2223-7747
language English
last_indexed 2024-03-10T03:25:51Z
publishDate 2021-12-01
publisher MDPI AG
record_format Article
series Plants
spelling doaj.art-33eefdb020834c0ba480dadd941c78242023-11-23T12:07:35ZengMDPI AGPlants2223-77472021-12-011119310.3390/plants11010093Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>So-Yon Park0Kohki Shimizu1Jocelyn Brown2Koh Aoki3James H. Westwood4School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA 24061, USAGraduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-1 Gakuen-cho, Naka-ku, Sakai 599-8531, JapanSchool of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA 24061, USAGraduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-1 Gakuen-cho, Naka-ku, Sakai 599-8531, JapanSchool of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA 24061, USA<i>Cuscuta</i> spp. are obligate parasites that connect to host vascular tissue using a haustorium. In addition to water, nutrients, and metabolites, a large number of mRNAs are bidirectionally exchanged between <i>Cuscuta</i> spp. and their hosts. This trans-specific movement of mRNAs raises questions about whether these molecules function in the recipient species. To address the possibility that mobile mRNAs are ultimately translated, we built upon recent studies that demonstrate a role for transfer RNA (tRNA)-like structures (TLSs) in enhancing mRNA systemic movement. <i>C. campestris</i> was grown on <i>Arabidopsis</i> that expressed a β-glucuronidase (<i>GUS</i>) reporter transgene either alone or in <i>GUS-tRNA</i> fusions. Histochemical staining revealed localization in tissue of <i>C. campestris</i> grown on <i>Arabidopsis</i> with <i>GUS-tRNA</i> fusions, but not in <i>C. campestris</i> grown on <i>Arabidopsis</i> with <i>GUS</i> alone. This corresponded with detection of <i>GUS</i> transcripts in <i>Cuscuta</i> on <i>Arabidopsis</i> with <i>GUS-tRNA</i>, but not in <i>C. campestris</i> on <i>Arabidopsis</i> with <i>GUS</i> alone. Similar results were obtained with <i>Arabidopsis</i> host plants expressing the same constructs containing an endoplasmic reticulum localization signal. In <i>C. campestris</i>, GUS activity was localized in the companion cells or phloem parenchyma cells adjacent to sieve tubes. We conclude that host-derived <i>GUS</i> mRNAs are translated in <i>C. campestris</i> and that the TLS fusion enhances RNA mobility in the host-parasite interactions.https://www.mdpi.com/2223-7747/11/1/93parasitic plants<i>Cuscuta</i>tRNAmobile mRNA
spellingShingle So-Yon Park
Kohki Shimizu
Jocelyn Brown
Koh Aoki
James H. Westwood
Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>
Plants
parasitic plants
<i>Cuscuta</i>
tRNA
mobile mRNA
title Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>
title_full Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>
title_fullStr Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>
title_full_unstemmed Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>
title_short Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant <i>Cuscuta campestris</i>
title_sort mobile host mrnas are translated to protein in the associated parasitic plant i cuscuta campestris i
topic parasitic plants
<i>Cuscuta</i>
tRNA
mobile mRNA
url https://www.mdpi.com/2223-7747/11/1/93
work_keys_str_mv AT soyonpark mobilehostmrnasaretranslatedtoproteinintheassociatedparasiticplanticuscutacampestrisi
AT kohkishimizu mobilehostmrnasaretranslatedtoproteinintheassociatedparasiticplanticuscutacampestrisi
AT jocelynbrown mobilehostmrnasaretranslatedtoproteinintheassociatedparasiticplanticuscutacampestrisi
AT kohaoki mobilehostmrnasaretranslatedtoproteinintheassociatedparasiticplanticuscutacampestrisi
AT jameshwestwood mobilehostmrnasaretranslatedtoproteinintheassociatedparasiticplanticuscutacampestrisi