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Dual Transcriptional Profiling of Carrot and ' Candidatus Liberibacter solanacearum' at Different Stages of Infection Suggests Complex Host-Pathogen Interaction

The interactions between the phloem-limited pathogen ' Liberibacter solanacearum' haplotype C and carrot ( subsp. ) were studied at 4, 5, and 9 weeks postinoculation (wpi), by combining dual RNA-Seq results with data on bacterial colonization and observations of the plant phenotype. In the...

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Published in:Molecular plant-microbe interactions 2021-11, Vol.34 (11), p.1281-1297
Main Authors: Wang, Jinhui, Haapalainen, Minna, Nissinen, Anne I, Pirhonen, Minna
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description The interactions between the phloem-limited pathogen ' Liberibacter solanacearum' haplotype C and carrot ( subsp. ) were studied at 4, 5, and 9 weeks postinoculation (wpi), by combining dual RNA-Seq results with data on bacterial colonization and observations of the plant phenotype. In the infected plants, genes involved in jasmonate biosynthesis, salicylate signaling, pathogen-associated molecular pattern- and effector-triggered immunity, and production of pathogenesis-related proteins were up-regulated. At 4 wpi, terpenoid synthesis-related genes were up-regulated, presumably as a response to the psyllid feeding, whereas at 5 and 9 wpi, genes involved in both the terpenoid and flavonoid production were down-regulated and phenylpropanoid genes were up-regulated. Chloroplast-related gene expression was down-regulated, in concordance with the observed yellowing of the infected plant leaves. Both the RNA-Seq data and electron microscopy suggested callose accumulation in the infected phloem vessels, likely to impair the transport of photosynthates, while phloem regeneration was suggested by the formation of new sieve cells and the upregulation of cell wall-related gene expression. The ' L. solanacearum' genes involved in replication, transcription, and translation were expressed at high levels at 4 and 5 wpi, whereas, at 9 wpi, the Flp pilus genes were highly expressed, suggesting adherence and reduced mobility of the bacteria. The ' L. solanacearum' genes encoding ATP and C4-dicarboxylate uptake were differentially expressed between the early and late infection stages, suggesting a change in the dependence on different host-derived energy sources. HPE1 effector and salicylate hydroxylase were expressed, presumably to suppress host cell death and salicylic acid-dependent defenses during the infection.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
doi_str_mv 10.1094/MPMI-10-20-0274-R
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In the infected plants, genes involved in jasmonate biosynthesis, salicylate signaling, pathogen-associated molecular pattern- and effector-triggered immunity, and production of pathogenesis-related proteins were up-regulated. At 4 wpi, terpenoid synthesis-related genes were up-regulated, presumably as a response to the psyllid feeding, whereas at 5 and 9 wpi, genes involved in both the terpenoid and flavonoid production were down-regulated and phenylpropanoid genes were up-regulated. Chloroplast-related gene expression was down-regulated, in concordance with the observed yellowing of the infected plant leaves. Both the RNA-Seq data and electron microscopy suggested callose accumulation in the infected phloem vessels, likely to impair the transport of photosynthates, while phloem regeneration was suggested by the formation of new sieve cells and the upregulation of cell wall-related gene expression. The ' L. solanacearum' genes involved in replication, transcription, and translation were expressed at high levels at 4 and 5 wpi, whereas, at 9 wpi, the Flp pilus genes were highly expressed, suggesting adherence and reduced mobility of the bacteria. The ' L. solanacearum' genes encoding ATP and C4-dicarboxylate uptake were differentially expressed between the early and late infection stages, suggesting a change in the dependence on different host-derived energy sources. HPE1 effector and salicylate hydroxylase were expressed, presumably to suppress host cell death and salicylic acid-dependent defenses during the infection.[Formula: see text] Copyright © 2021 The Author(s). 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In the infected plants, genes involved in jasmonate biosynthesis, salicylate signaling, pathogen-associated molecular pattern- and effector-triggered immunity, and production of pathogenesis-related proteins were up-regulated. At 4 wpi, terpenoid synthesis-related genes were up-regulated, presumably as a response to the psyllid feeding, whereas at 5 and 9 wpi, genes involved in both the terpenoid and flavonoid production were down-regulated and phenylpropanoid genes were up-regulated. Chloroplast-related gene expression was down-regulated, in concordance with the observed yellowing of the infected plant leaves. Both the RNA-Seq data and electron microscopy suggested callose accumulation in the infected phloem vessels, likely to impair the transport of photosynthates, while phloem regeneration was suggested by the formation of new sieve cells and the upregulation of cell wall-related gene expression. The ' L. solanacearum' genes involved in replication, transcription, and translation were expressed at high levels at 4 and 5 wpi, whereas, at 9 wpi, the Flp pilus genes were highly expressed, suggesting adherence and reduced mobility of the bacteria. The ' L. solanacearum' genes encoding ATP and C4-dicarboxylate uptake were differentially expressed between the early and late infection stages, suggesting a change in the dependence on different host-derived energy sources. HPE1 effector and salicylate hydroxylase were expressed, presumably to suppress host cell death and salicylic acid-dependent defenses during the infection.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.</description><subject>Animals</subject><subject>Biosynthesis</subject><subject>Candidatus Liberibacter solanacearum</subject><subject>Carrots</subject><subject>Cell death</subject><subject>Cell walls</subject><subject>Chloroplasts</subject><subject>Daucus carota</subject><subject>Daucus carota - genetics</subject><subject>Daucus carota - microbiology</subject><subject>Daucus carota sativus</subject><subject>dual RNA-Seq</subject><subject>Electron microscopy</subject><subject>Energy sources</subject><subject>Flavonoids</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Haplotypes</subject><subject>Hemiptera</subject><subject>Host-pathogen interactions</subject><subject>Host-Pathogen Interactions - genetics</subject><subject>Hydroxylase</subject><subject>Infections</subject><subject>Jasmonic acid</subject><subject>Liberibacter - genetics</subject><subject>Liberibacter - pathogenicity</subject><subject>Pathogenesis</subject><subject>Pathogenesis-related proteins</subject><subject>Pathogens</subject><subject>Phenotypes</subject><subject>Phloem</subject><subject>Photosynthates</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - microbiology</subject><subject>plant hormones</subject><subject>plant-pathogen interactions</subject><subject>Regeneration</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Salicylate hydroxylase</subject><subject>Salicylic acid</subject><subject>Transcription</subject><subject>Trioza apicalis</subject><subject>Yellowing</subject><issn>0894-0282</issn><issn>1943-7706</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpdkstu1DAUhiMEokPhAdggSyzKJuBLHDtLNAU60lSM2rK2TnwJHmXiwXak8jY8Kk6ndMHKOr-_8_ty_qp6S_BHgrvm0_XuelMTXFNcYyqa-uZZtSJdw2ohcPu8WmHZNWVH0rPqVUp7jEnXcv6yOmMNI50QbFX9uZxhRHcRpqSjP2YfplLvYnB-9NOAgkNriDFkBJNBF6WYjDeQ54S2vrfR96CzjSiFESbQFuJ8uECQ0aV3zkY7ZXSbYbBpcdpMzurlCHQ7D0XLCa3D4Tjae3QVUq53kH-GwU4FLJ7wgL6uXjgYk33zuJ5XP75-uVtf1dvv3zbrz9taN0zmWnPZS0OM64ShwklNgIPlPQMq2p60hmroTSco447yImHHCMMd4wwTrjk7rzYnXxNgr47RHyD-VgG8ehBCHBTE7PVoFePCSmuZcbRrOJG9g1YazhpKLTApiteHk9cxhl9zeac6-KTtWL7IhjkpynlbOInbgr7_D92HOZYZFKolrZQdxk2hyInSMaQUrXu6IMFqiYJaorAUFKslCuqm9Lx7dJ77gzVPHf9mz_4CXtOwiw</recordid><startdate>202111</startdate><enddate>202111</enddate><creator>Wang, Jinhui</creator><creator>Haapalainen, Minna</creator><creator>Nissinen, Anne I</creator><creator>Pirhonen, Minna</creator><general>American Phytopathological Society</general><general>The American Phytopathological Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>K9.</scope><scope>7X8</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5249-563X</orcidid><orcidid>https://orcid.org/0000-0002-4328-984X</orcidid></search><sort><creationdate>202111</creationdate><title>Dual Transcriptional Profiling of Carrot and ' Candidatus Liberibacter solanacearum' at Different Stages of Infection Suggests Complex Host-Pathogen Interaction</title><author>Wang, Jinhui ; 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Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Molecular plant-microbe interactions</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Jinhui</au><au>Haapalainen, Minna</au><au>Nissinen, Anne I</au><au>Pirhonen, Minna</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dual Transcriptional Profiling of Carrot and ' Candidatus Liberibacter solanacearum' at Different Stages of Infection Suggests Complex Host-Pathogen Interaction</atitle><jtitle>Molecular plant-microbe interactions</jtitle><addtitle>Mol Plant Microbe Interact</addtitle><date>2021-11</date><risdate>2021</risdate><volume>34</volume><issue>11</issue><spage>1281</spage><epage>1297</epage><pages>1281-1297</pages><issn>0894-0282</issn><eissn>1943-7706</eissn><abstract>The interactions between the phloem-limited pathogen ' Liberibacter solanacearum' haplotype C and carrot ( subsp. ) were studied at 4, 5, and 9 weeks postinoculation (wpi), by combining dual RNA-Seq results with data on bacterial colonization and observations of the plant phenotype. In the infected plants, genes involved in jasmonate biosynthesis, salicylate signaling, pathogen-associated molecular pattern- and effector-triggered immunity, and production of pathogenesis-related proteins were up-regulated. At 4 wpi, terpenoid synthesis-related genes were up-regulated, presumably as a response to the psyllid feeding, whereas at 5 and 9 wpi, genes involved in both the terpenoid and flavonoid production were down-regulated and phenylpropanoid genes were up-regulated. Chloroplast-related gene expression was down-regulated, in concordance with the observed yellowing of the infected plant leaves. Both the RNA-Seq data and electron microscopy suggested callose accumulation in the infected phloem vessels, likely to impair the transport of photosynthates, while phloem regeneration was suggested by the formation of new sieve cells and the upregulation of cell wall-related gene expression. The ' L. solanacearum' genes involved in replication, transcription, and translation were expressed at high levels at 4 and 5 wpi, whereas, at 9 wpi, the Flp pilus genes were highly expressed, suggesting adherence and reduced mobility of the bacteria. The ' L. solanacearum' genes encoding ATP and C4-dicarboxylate uptake were differentially expressed between the early and late infection stages, suggesting a change in the dependence on different host-derived energy sources. HPE1 effector and salicylate hydroxylase were expressed, presumably to suppress host cell death and salicylic acid-dependent defenses during the infection.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.</abstract><cop>United States</cop><pub>American Phytopathological Society</pub><pmid>34319773</pmid><doi>10.1094/MPMI-10-20-0274-R</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-5249-563X</orcidid><orcidid>https://orcid.org/0000-0002-4328-984X</orcidid><oa>free_for_read</oa></addata></record>
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subjects Animals
Biosynthesis
Candidatus Liberibacter solanacearum
Carrots
Cell death
Cell walls
Chloroplasts
Daucus carota
Daucus carota - genetics
Daucus carota - microbiology
Daucus carota sativus
dual RNA-Seq
Electron microscopy
Energy sources
Flavonoids
Gene expression
Genes
Haplotypes
Hemiptera
Host-pathogen interactions
Host-Pathogen Interactions - genetics
Hydroxylase
Infections
Jasmonic acid
Liberibacter - genetics
Liberibacter - pathogenicity
Pathogenesis
Pathogenesis-related proteins
Pathogens
Phenotypes
Phloem
Photosynthates
Plant Diseases - genetics
Plant Diseases - microbiology
plant hormones
plant-pathogen interactions
Regeneration
Ribonucleic acid
RNA
Salicylate hydroxylase
Salicylic acid
Transcription
Trioza apicalis
Yellowing
title Dual Transcriptional Profiling of Carrot and ' Candidatus Liberibacter solanacearum' at Different Stages of Infection Suggests Complex Host-Pathogen Interaction
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