Low nitrate under waterlogging triggers exodermal suberization to form a barrier to radial oxygen loss in rice roots

Abstract To acclimate to hypoxic waterlogged conditions, the roots of wetland plants form a radial oxygen loss (ROL) barrier that can promote oxygen diffusion to the root tips. We hypothesized that the low-nitrate concentrations that occur after molecular oxygen is consumed in waterlogged soils are...

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Veröffentlicht in:Plant physiology (Bethesda) 2024-09, Vol.196 (1), p.551-563
Hauptverfasser: Shiono, Katsuhiro, Ejiri, Masato, Sawazaki, Yuto, Egishi, Yuka, Tsunoda, Tomonori
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creator Shiono, Katsuhiro
Ejiri, Masato
Sawazaki, Yuto
Egishi, Yuka
Tsunoda, Tomonori
description Abstract To acclimate to hypoxic waterlogged conditions, the roots of wetland plants form a radial oxygen loss (ROL) barrier that can promote oxygen diffusion to the root tips. We hypothesized that the low-nitrate concentrations that occur after molecular oxygen is consumed in waterlogged soils are an environmental trigger for ROL barrier formation in rice (Oryza sativa). We previously identified 128 tissue-specific up/downregulated genes during rice ROL barrier formation. The RiceXPro database showed that many of these genes were differentially regulated in response to nitrogen deficiency. Therefore, we assessed changes in the concentrations of ionic species of nitrogen under stagnant conditions, i.e. in a nutrient solution that mimics waterlogged soil conditions, and examined the effects of an increase or decrease of nitrate in the nutrient solution on ROL barrier formation and exodermal suberization. Preventing nitrate deficiency in the stagnant nutrient solution suppressed the formation of an ROL barrier. Conversely, a decrease in nitrate strongly induced ROL barrier formation, even under aerated conditions. In parallel with ROL barrier formation, suberin lamellae formed at the exodermis. Nitrate deficiency also promoted aerenchyma formation and the enlargement of root diameters. These findings suggest that the severe decline of nitrates under waterlogged conditions is an environmental cue for exodermal suberization to form an ROL barrier in rice roots. Low-nitrate concentrations occur after molecular oxygen is consumed in waterlogged soils and are an environmental trigger for forming a root barrier to radial oxygen loss in rice roots.
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We hypothesized that the low-nitrate concentrations that occur after molecular oxygen is consumed in waterlogged soils are an environmental trigger for ROL barrier formation in rice (Oryza sativa). We previously identified 128 tissue-specific up/downregulated genes during rice ROL barrier formation. The RiceXPro database showed that many of these genes were differentially regulated in response to nitrogen deficiency. Therefore, we assessed changes in the concentrations of ionic species of nitrogen under stagnant conditions, i.e. in a nutrient solution that mimics waterlogged soil conditions, and examined the effects of an increase or decrease of nitrate in the nutrient solution on ROL barrier formation and exodermal suberization. Preventing nitrate deficiency in the stagnant nutrient solution suppressed the formation of an ROL barrier. Conversely, a decrease in nitrate strongly induced ROL barrier formation, even under aerated conditions. In parallel with ROL barrier formation, suberin lamellae formed at the exodermis. Nitrate deficiency also promoted aerenchyma formation and the enlargement of root diameters. These findings suggest that the severe decline of nitrates under waterlogged conditions is an environmental cue for exodermal suberization to form an ROL barrier in rice roots. Low-nitrate concentrations occur after molecular oxygen is consumed in waterlogged soils and are an environmental trigger for forming a root barrier to radial oxygen loss in rice roots.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1093/plphys/kiae278</identifier><identifier>PMID: 38761404</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Gene Expression Regulation, Plant ; Lipids ; Nitrates - metabolism ; Nitrogen - metabolism ; Oryza - genetics ; Oryza - growth &amp; development ; Oryza - metabolism ; Oryza - physiology ; Oxygen - metabolism ; Plant Roots - genetics ; Plant Roots - growth &amp; development ; Plant Roots - metabolism ; Soil - chemistry ; Water - metabolism</subject><ispartof>Plant physiology (Bethesda), 2024-09, Vol.196 (1), p.551-563</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. 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We hypothesized that the low-nitrate concentrations that occur after molecular oxygen is consumed in waterlogged soils are an environmental trigger for ROL barrier formation in rice (Oryza sativa). We previously identified 128 tissue-specific up/downregulated genes during rice ROL barrier formation. The RiceXPro database showed that many of these genes were differentially regulated in response to nitrogen deficiency. Therefore, we assessed changes in the concentrations of ionic species of nitrogen under stagnant conditions, i.e. in a nutrient solution that mimics waterlogged soil conditions, and examined the effects of an increase or decrease of nitrate in the nutrient solution on ROL barrier formation and exodermal suberization. Preventing nitrate deficiency in the stagnant nutrient solution suppressed the formation of an ROL barrier. Conversely, a decrease in nitrate strongly induced ROL barrier formation, even under aerated conditions. In parallel with ROL barrier formation, suberin lamellae formed at the exodermis. Nitrate deficiency also promoted aerenchyma formation and the enlargement of root diameters. These findings suggest that the severe decline of nitrates under waterlogged conditions is an environmental cue for exodermal suberization to form an ROL barrier in rice roots. Low-nitrate concentrations occur after molecular oxygen is consumed in waterlogged soils and are an environmental trigger for forming a root barrier to radial oxygen loss in rice roots.</description><subject>Gene Expression Regulation, Plant</subject><subject>Lipids</subject><subject>Nitrates - metabolism</subject><subject>Nitrogen - metabolism</subject><subject>Oryza - genetics</subject><subject>Oryza - growth &amp; development</subject><subject>Oryza - metabolism</subject><subject>Oryza - physiology</subject><subject>Oxygen - metabolism</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - growth &amp; development</subject><subject>Plant Roots - metabolism</subject><subject>Soil - chemistry</subject><subject>Water - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkL1PwzAQxS0EouVjZUQeYWixk9ixR4T4kiqxwBzZjhMMSRzOjmj56zFqYWW6p7vfezo9hM4oWVIi86uxG1834erdKZuVYg_NKcuzRcYKsY_mhCRNhJAzdBTCGyGE5rQ4RLNclJwWpJijuPKfeHARVLR4GmoL-DNJ6HzbuqHFEVzbWgjYrn069qrDYdIW3JeKzg84etx46LHCWgG4ZE8bULVLoF9vWjvgzoeA3YDBGYvB-xhO0EGjumBPd_MYvdzdPt88LFZP948316uFyWgRF0ZomutaCVLKpmSEN1ITZXOuS0YZk6SmxkhORK1MoxsmRM24EKaRgutMqvwYXWxzR_Afkw2x6l0wtuvUYP0Uqpwwznkmiyyhyy1qIL0LtqlGcL2CTUVJ9dN0tW262jWdDOe77En3tv7Df6tNwOUW8NP4X9g3pzqNSw</recordid><startdate>20240902</startdate><enddate>20240902</enddate><creator>Shiono, Katsuhiro</creator><creator>Ejiri, Masato</creator><creator>Sawazaki, Yuto</creator><creator>Egishi, Yuka</creator><creator>Tsunoda, Tomonori</creator><general>Oxford University Press</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>7X8</scope><orcidid>https://orcid.org/0000-0001-6838-8740</orcidid><orcidid>https://orcid.org/0009-0009-5802-1975</orcidid><orcidid>https://orcid.org/0009-0005-1362-7376</orcidid><orcidid>https://orcid.org/0000-0002-1163-2893</orcidid><orcidid>https://orcid.org/0000-0001-7897-978X</orcidid></search><sort><creationdate>20240902</creationdate><title>Low nitrate under waterlogging triggers exodermal suberization to form a barrier to radial oxygen loss in rice roots</title><author>Shiono, Katsuhiro ; Ejiri, Masato ; Sawazaki, Yuto ; Egishi, Yuka ; Tsunoda, Tomonori</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c214t-c8b13bda8079f7506f9b0ae36b7515590d1cc9608dacfbf588d5688cf986b29a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Gene Expression Regulation, Plant</topic><topic>Lipids</topic><topic>Nitrates - metabolism</topic><topic>Nitrogen - metabolism</topic><topic>Oryza - genetics</topic><topic>Oryza - growth &amp; development</topic><topic>Oryza - metabolism</topic><topic>Oryza - physiology</topic><topic>Oxygen - metabolism</topic><topic>Plant Roots - genetics</topic><topic>Plant Roots - growth &amp; development</topic><topic>Plant Roots - metabolism</topic><topic>Soil - chemistry</topic><topic>Water - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shiono, Katsuhiro</creatorcontrib><creatorcontrib>Ejiri, Masato</creatorcontrib><creatorcontrib>Sawazaki, Yuto</creatorcontrib><creatorcontrib>Egishi, Yuka</creatorcontrib><creatorcontrib>Tsunoda, Tomonori</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shiono, Katsuhiro</au><au>Ejiri, Masato</au><au>Sawazaki, Yuto</au><au>Egishi, Yuka</au><au>Tsunoda, Tomonori</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Low nitrate under waterlogging triggers exodermal suberization to form a barrier to radial oxygen loss in rice roots</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2024-09-02</date><risdate>2024</risdate><volume>196</volume><issue>1</issue><spage>551</spage><epage>563</epage><pages>551-563</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><abstract>Abstract To acclimate to hypoxic waterlogged conditions, the roots of wetland plants form a radial oxygen loss (ROL) barrier that can promote oxygen diffusion to the root tips. 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source MEDLINE; Oxford University Press Journals All Titles (1996-Current)
subjects Gene Expression Regulation, Plant
Lipids
Nitrates - metabolism
Nitrogen - metabolism
Oryza - genetics
Oryza - growth & development
Oryza - metabolism
Oryza - physiology
Oxygen - metabolism
Plant Roots - genetics
Plant Roots - growth & development
Plant Roots - metabolism
Soil - chemistry
Water - metabolism
title Low nitrate under waterlogging triggers exodermal suberization to form a barrier to radial oxygen loss in rice roots
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