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Apoplast-symplast compartmentalization and functional traits of iron and aluminum in promeristematic tissues of nematode induced galls on Miconia spp
The nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda) have promeristematic capacity, which may turn these galls into sinks of Al on their Melastomataceae Al-accumulating hosts. Such a sink of Al may affect gall growth and mineral nutrient intake. Based on the fact that galls...
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Published in: | Plant physiology and biochemistry 2020-09, Vol.154, p.360-368 |
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description | The nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda) have promeristematic capacity, which may turn these galls into sinks of Al on their Melastomataceae Al-accumulating hosts. Such a sink of Al may affect gall growth and mineral nutrient intake. Based on the fact that galls are good models for plant developmental studies, we aimed to understand how Al-accumulating host plants in the Cerrado environment deal with Al toxicity in subcellular levels. Here, we used the ICP-OES method to check the variations on mineral nutrients, and the morin, hematoxylin, and Prussian blue stainings for Al and Fe histolocalization in galls induced on four Miconia species of the Brazilian Cerrado. We confirmed the new Al-accumulating feature for two Miconia species of the Cerrado environment. Furthermore, we found that Al accumulates in lesser concentrations in gall tissues than in non-galled tissues of the Miconia hosts. Staining methods indicated that the polyphenols avoid Al-binding to the apoplast and the nucleolus of the promeristematic cells, and mediated its binding to parenchyma cell walls. As well, we inferred that Fe3+ is transported by xylem and stored in gall parenchyma, where it is reduced to Fe2+, being available in gall nutritive cells. Our results demonstrated an Al compartmentalization between the apoplast and symplast of the inner cell layers in galls, as well as indicated the phenolics action against Al-toxicity and toward Fe availability for the diet of Ditylenchus gallaeformans.
•Ditylenchus gallaeformans induce leaf galls with promeristematic capacity on Al-accumulating host plants.•Al is not associated with the walls of the promeristematic cells in gall tissues.•Ditylenchus gallaeformans manipulate its host-plants to acquire Fe supply.•Polyphenols act in the Fe disponibilization to the nematodes diet, and the Al compartmentalization in gall tissues. |
doi_str_mv | 10.1016/j.plaphy.2020.06.031 |
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•Ditylenchus gallaeformans induce leaf galls with promeristematic capacity on Al-accumulating host plants.•Al is not associated with the walls of the promeristematic cells in gall tissues.•Ditylenchus gallaeformans manipulate its host-plants to acquire Fe supply.•Polyphenols act in the Fe disponibilization to the nematodes diet, and the Al compartmentalization in gall tissues.</description><identifier>ISSN: 0981-9428</identifier><identifier>EISSN: 1873-2690</identifier><identifier>DOI: 10.1016/j.plaphy.2020.06.031</identifier><language>eng</language><publisher>Elsevier Masson SAS</publisher><subject>aluminum ; apoplast ; Brazilian cerrado ; cell nucleolus ; cerrado ; diet ; Ditylenchus ; Fe supply ; iron ; Melastomataceae ; Metal-rich galls ; Miconia ; nutrient intake ; plant physiology ; Polyphenols ; Reactive oxygen species ; species ; symplast ; toxicity ; xylem</subject><ispartof>Plant physiology and biochemistry, 2020-09, Vol.154, p.360-368</ispartof><rights>2020 Elsevier Masson SAS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c372t-58496f94c73272edaea3cd26b2b484255ce8c3267de77f192fe34b282ec63fe73</citedby><cites>FETCH-LOGICAL-c372t-58496f94c73272edaea3cd26b2b484255ce8c3267de77f192fe34b282ec63fe73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids></links><search><creatorcontrib>Arriola, Ígor Abba</creatorcontrib><creatorcontrib>Figueiredo, Maurílio Assis</creatorcontrib><creatorcontrib>Boanares, Daniela</creatorcontrib><creatorcontrib>França, Marcel Giovanni Costa</creatorcontrib><creatorcontrib>Isaias, Rosy Mary dos Santos</creatorcontrib><title>Apoplast-symplast compartmentalization and functional traits of iron and aluminum in promeristematic tissues of nematode induced galls on Miconia spp</title><title>Plant physiology and biochemistry</title><description>The nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda) have promeristematic capacity, which may turn these galls into sinks of Al on their Melastomataceae Al-accumulating hosts. Such a sink of Al may affect gall growth and mineral nutrient intake. Based on the fact that galls are good models for plant developmental studies, we aimed to understand how Al-accumulating host plants in the Cerrado environment deal with Al toxicity in subcellular levels. Here, we used the ICP-OES method to check the variations on mineral nutrients, and the morin, hematoxylin, and Prussian blue stainings for Al and Fe histolocalization in galls induced on four Miconia species of the Brazilian Cerrado. We confirmed the new Al-accumulating feature for two Miconia species of the Cerrado environment. Furthermore, we found that Al accumulates in lesser concentrations in gall tissues than in non-galled tissues of the Miconia hosts. Staining methods indicated that the polyphenols avoid Al-binding to the apoplast and the nucleolus of the promeristematic cells, and mediated its binding to parenchyma cell walls. As well, we inferred that Fe3+ is transported by xylem and stored in gall parenchyma, where it is reduced to Fe2+, being available in gall nutritive cells. Our results demonstrated an Al compartmentalization between the apoplast and symplast of the inner cell layers in galls, as well as indicated the phenolics action against Al-toxicity and toward Fe availability for the diet of Ditylenchus gallaeformans.
•Ditylenchus gallaeformans induce leaf galls with promeristematic capacity on Al-accumulating host plants.•Al is not associated with the walls of the promeristematic cells in gall tissues.•Ditylenchus gallaeformans manipulate its host-plants to acquire Fe supply.•Polyphenols act in the Fe disponibilization to the nematodes diet, and the Al compartmentalization in gall tissues.</description><subject>aluminum</subject><subject>apoplast</subject><subject>Brazilian cerrado</subject><subject>cell nucleolus</subject><subject>cerrado</subject><subject>diet</subject><subject>Ditylenchus</subject><subject>Fe supply</subject><subject>iron</subject><subject>Melastomataceae</subject><subject>Metal-rich galls</subject><subject>Miconia</subject><subject>nutrient intake</subject><subject>plant physiology</subject><subject>Polyphenols</subject><subject>Reactive oxygen species</subject><subject>species</subject><subject>symplast</subject><subject>toxicity</subject><subject>xylem</subject><issn>0981-9428</issn><issn>1873-2690</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNqFkc1u3CAUhVGVSp2mfYMuWGZjl78BexMpitK0UqJs2jVi8HXLiB8HcKTJe_R9y2SybiQkuNzvHF04CH2hpKeEyq_7fvFm-XPoGWGkJ7InnL5DGzoo3jE5kjO0IeNAu1Gw4QP6WMqeEMKE4hv092pJTVxqVw7h5YBtCovJNUCsxrtnU12K2MQJz2u0x8J4XLNxteA0Y5dfu8avwcU1YBfxklOA7EqF0OQWV1fKCi98PF6lCRo2rRYm_Nt43zoR3zubojO4LMsn9H42vsDn1_0c_fp28_P6e3f3cPvj-uqus1yx2m0HMcp5FFZxphhMBgy3E5M7thODYNuthcFyJtUESs10ZDNwsWMDAyv5DIqfo4uTbxv4sQ1YdXDFgvcmQlqLbhaMENHW26gQVJJRENZQcUJtTqVkmPWSXTD5oCnRx8D0Xp8C08fANJG6BdZklycZtBc_Oci6WAex_ZHLYKuekvu_wT8PrqTh</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Arriola, Ígor Abba</creator><creator>Figueiredo, Maurílio Assis</creator><creator>Boanares, Daniela</creator><creator>França, Marcel Giovanni Costa</creator><creator>Isaias, Rosy Mary dos Santos</creator><general>Elsevier Masson SAS</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>202009</creationdate><title>Apoplast-symplast compartmentalization and functional traits of iron and aluminum in promeristematic tissues of nematode induced galls on Miconia spp</title><author>Arriola, Ígor Abba ; Figueiredo, Maurílio Assis ; Boanares, Daniela ; França, Marcel Giovanni Costa ; Isaias, Rosy Mary dos Santos</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c372t-58496f94c73272edaea3cd26b2b484255ce8c3267de77f192fe34b282ec63fe73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>aluminum</topic><topic>apoplast</topic><topic>Brazilian cerrado</topic><topic>cell nucleolus</topic><topic>cerrado</topic><topic>diet</topic><topic>Ditylenchus</topic><topic>Fe supply</topic><topic>iron</topic><topic>Melastomataceae</topic><topic>Metal-rich galls</topic><topic>Miconia</topic><topic>nutrient intake</topic><topic>plant physiology</topic><topic>Polyphenols</topic><topic>Reactive oxygen species</topic><topic>species</topic><topic>symplast</topic><topic>toxicity</topic><topic>xylem</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Arriola, Ígor Abba</creatorcontrib><creatorcontrib>Figueiredo, Maurílio Assis</creatorcontrib><creatorcontrib>Boanares, Daniela</creatorcontrib><creatorcontrib>França, Marcel Giovanni Costa</creatorcontrib><creatorcontrib>Isaias, Rosy Mary dos Santos</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Plant physiology and biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Arriola, Ígor Abba</au><au>Figueiredo, Maurílio Assis</au><au>Boanares, Daniela</au><au>França, Marcel Giovanni Costa</au><au>Isaias, Rosy Mary dos Santos</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Apoplast-symplast compartmentalization and functional traits of iron and aluminum in promeristematic tissues of nematode induced galls on Miconia spp</atitle><jtitle>Plant physiology and biochemistry</jtitle><date>2020-09</date><risdate>2020</risdate><volume>154</volume><spage>360</spage><epage>368</epage><pages>360-368</pages><issn>0981-9428</issn><eissn>1873-2690</eissn><abstract>The nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda) have promeristematic capacity, which may turn these galls into sinks of Al on their Melastomataceae Al-accumulating hosts. Such a sink of Al may affect gall growth and mineral nutrient intake. Based on the fact that galls are good models for plant developmental studies, we aimed to understand how Al-accumulating host plants in the Cerrado environment deal with Al toxicity in subcellular levels. Here, we used the ICP-OES method to check the variations on mineral nutrients, and the morin, hematoxylin, and Prussian blue stainings for Al and Fe histolocalization in galls induced on four Miconia species of the Brazilian Cerrado. We confirmed the new Al-accumulating feature for two Miconia species of the Cerrado environment. Furthermore, we found that Al accumulates in lesser concentrations in gall tissues than in non-galled tissues of the Miconia hosts. Staining methods indicated that the polyphenols avoid Al-binding to the apoplast and the nucleolus of the promeristematic cells, and mediated its binding to parenchyma cell walls. As well, we inferred that Fe3+ is transported by xylem and stored in gall parenchyma, where it is reduced to Fe2+, being available in gall nutritive cells. Our results demonstrated an Al compartmentalization between the apoplast and symplast of the inner cell layers in galls, as well as indicated the phenolics action against Al-toxicity and toward Fe availability for the diet of Ditylenchus gallaeformans.
•Ditylenchus gallaeformans induce leaf galls with promeristematic capacity on Al-accumulating host plants.•Al is not associated with the walls of the promeristematic cells in gall tissues.•Ditylenchus gallaeformans manipulate its host-plants to acquire Fe supply.•Polyphenols act in the Fe disponibilization to the nematodes diet, and the Al compartmentalization in gall tissues.</abstract><pub>Elsevier Masson SAS</pub><doi>10.1016/j.plaphy.2020.06.031</doi><tpages>9</tpages></addata></record> |
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subjects | aluminum apoplast Brazilian cerrado cell nucleolus cerrado diet Ditylenchus Fe supply iron Melastomataceae Metal-rich galls Miconia nutrient intake plant physiology Polyphenols Reactive oxygen species species symplast toxicity xylem |
title | Apoplast-symplast compartmentalization and functional traits of iron and aluminum in promeristematic tissues of nematode induced galls on Miconia spp |
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