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Raffinose positively regulates maize drought tolerance by reducing leaf transpiration

SUMMARY Drought stress is one of the major constraints of global crop production. Raffinose, a non‐reducing trisaccharide, has been considered to regulate positively the plant drought stress tolerance; however, evidence that augmenting raffinose production in leaves results in enhanced plant drought...

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Published in:The Plant journal : for cell and molecular biology 2023-04, Vol.114 (1), p.55-67
Main Authors: Liu, Ying, Li, Tao, Zhang, Chunxia, Zhang, Wenli, Deng, Nan, Dirk, Lynnette M. A., Downie, A. Bruce, Zhao, Tianyong
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container_title The Plant journal : for cell and molecular biology
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Li, Tao
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Zhang, Wenli
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Dirk, Lynnette M. A.
Downie, A. Bruce
Zhao, Tianyong
description SUMMARY Drought stress is one of the major constraints of global crop production. Raffinose, a non‐reducing trisaccharide, has been considered to regulate positively the plant drought stress tolerance; however, evidence that augmenting raffinose production in leaves results in enhanced plant drought stress tolerance is lacking. The biochemical mechanism through which raffinose might act to mitigate plant drought stress remains unidentified. ZmRAFS encodes Zea mays RAFFINOSE SYNTHASE, a key enzyme that transfers galactose from the galactoside galactinol to sucrose for raffinose production. Overexpression of ZmRAFS in maize increased the RAFS protein and the raffinose content and decreased the water loss of leaves and enhanced plant drought stress tolerance. The biomass of the ZmRAFS overexpressing plants was similar to that of non‐transgenic control plants when grown under optimal conditions, but was significantly greater than that of non‐transgenic plants when grown under drought stress conditions. In contrast, the percentage of water loss of the detached leaves from two independent zmrafs mutant lines, incapable of synthesizing raffinose, was greater than that from null segregant controls and this phenomenon was partially rescued by supplementation of raffinose to detached zmrafs leaves. In addition, while there were differences in water loss among different maize lines, there was no difference in stomata density or aperture. Taken together, our work demonstrated that overexpression of the ZmRAFS gene in maize, in contrast to Arabidopsis, increased the raffinose content in leaves, assisted the leaf to retain water, and enhanced the plant drought stress tolerance without causing a detectable growth penalty. Significance Statement Raffinose has been positively correlated with drought tolerance but its mechanism of action remains obscure. The amounts of raffinose increased in leaves of maize plants constitutively overexpressing its RAFFINOSE SYNTHASE gene, which then assisted the leaf to retain water, and enhanced the plant drought stress tolerance without a growth penalty. Raffinose exerts its protective effect independent of leaf stomata density, and aperture or the cell plasma membrane structure; presumably through its in vitro demonstrable physical, hygroscopic properties.
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A. ; Downie, A. Bruce ; Zhao, Tianyong</creator><creatorcontrib>Liu, Ying ; Li, Tao ; Zhang, Chunxia ; Zhang, Wenli ; Deng, Nan ; Dirk, Lynnette M. A. ; Downie, A. Bruce ; Zhao, Tianyong</creatorcontrib><description>SUMMARY Drought stress is one of the major constraints of global crop production. Raffinose, a non‐reducing trisaccharide, has been considered to regulate positively the plant drought stress tolerance; however, evidence that augmenting raffinose production in leaves results in enhanced plant drought stress tolerance is lacking. The biochemical mechanism through which raffinose might act to mitigate plant drought stress remains unidentified. ZmRAFS encodes Zea mays RAFFINOSE SYNTHASE, a key enzyme that transfers galactose from the galactoside galactinol to sucrose for raffinose production. Overexpression of ZmRAFS in maize increased the RAFS protein and the raffinose content and decreased the water loss of leaves and enhanced plant drought stress tolerance. The biomass of the ZmRAFS overexpressing plants was similar to that of non‐transgenic control plants when grown under optimal conditions, but was significantly greater than that of non‐transgenic plants when grown under drought stress conditions. In contrast, the percentage of water loss of the detached leaves from two independent zmrafs mutant lines, incapable of synthesizing raffinose, was greater than that from null segregant controls and this phenomenon was partially rescued by supplementation of raffinose to detached zmrafs leaves. In addition, while there were differences in water loss among different maize lines, there was no difference in stomata density or aperture. Taken together, our work demonstrated that overexpression of the ZmRAFS gene in maize, in contrast to Arabidopsis, increased the raffinose content in leaves, assisted the leaf to retain water, and enhanced the plant drought stress tolerance without causing a detectable growth penalty. Significance Statement Raffinose has been positively correlated with drought tolerance but its mechanism of action remains obscure. The amounts of raffinose increased in leaves of maize plants constitutively overexpressing its RAFFINOSE SYNTHASE gene, which then assisted the leaf to retain water, and enhanced the plant drought stress tolerance without a growth penalty. Raffinose exerts its protective effect independent of leaf stomata density, and aperture or the cell plasma membrane structure; presumably through its in vitro demonstrable physical, hygroscopic properties.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16116</identifier><identifier>PMID: 36703577</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis - metabolism ; carbohydrate metabolism ; Corn ; Crop production ; Drought Resistance ; drought stress ; Droughts ; Galactose ; Galactosides ; Gene Expression Regulation, Plant ; Leaves ; maize (Zea mays) ; Oligosaccharides ; Plant Leaves - genetics ; Plant Leaves - metabolism ; Plants ; Plants (botany) ; Plants, Genetically Modified - metabolism ; Raffinose ; RAFFINOSE SYNTHASE ; Stomata ; Stress, Physiological - genetics ; Sucrose ; Transgenic plants ; Transpiration ; Water - metabolism ; Water loss ; Zea mays ; Zea mays - metabolism</subject><ispartof>The Plant journal : for cell and molecular biology, 2023-04, Vol.114 (1), p.55-67</ispartof><rights>2023 Society for Experimental Biology and John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2023 Society for Experimental Biology and John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3886-9f7012d030cd91544cae8464e0d265dfe8e754385fb1be3cf03c06175e0412a53</citedby><cites>FETCH-LOGICAL-c3886-9f7012d030cd91544cae8464e0d265dfe8e754385fb1be3cf03c06175e0412a53</cites><orcidid>0000-0002-1278-2842</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27922,27923</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36703577$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Ying</creatorcontrib><creatorcontrib>Li, Tao</creatorcontrib><creatorcontrib>Zhang, Chunxia</creatorcontrib><creatorcontrib>Zhang, Wenli</creatorcontrib><creatorcontrib>Deng, Nan</creatorcontrib><creatorcontrib>Dirk, Lynnette M. A.</creatorcontrib><creatorcontrib>Downie, A. Bruce</creatorcontrib><creatorcontrib>Zhao, Tianyong</creatorcontrib><title>Raffinose positively regulates maize drought tolerance by reducing leaf transpiration</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY Drought stress is one of the major constraints of global crop production. Raffinose, a non‐reducing trisaccharide, has been considered to regulate positively the plant drought stress tolerance; however, evidence that augmenting raffinose production in leaves results in enhanced plant drought stress tolerance is lacking. The biochemical mechanism through which raffinose might act to mitigate plant drought stress remains unidentified. ZmRAFS encodes Zea mays RAFFINOSE SYNTHASE, a key enzyme that transfers galactose from the galactoside galactinol to sucrose for raffinose production. Overexpression of ZmRAFS in maize increased the RAFS protein and the raffinose content and decreased the water loss of leaves and enhanced plant drought stress tolerance. The biomass of the ZmRAFS overexpressing plants was similar to that of non‐transgenic control plants when grown under optimal conditions, but was significantly greater than that of non‐transgenic plants when grown under drought stress conditions. In contrast, the percentage of water loss of the detached leaves from two independent zmrafs mutant lines, incapable of synthesizing raffinose, was greater than that from null segregant controls and this phenomenon was partially rescued by supplementation of raffinose to detached zmrafs leaves. In addition, while there were differences in water loss among different maize lines, there was no difference in stomata density or aperture. Taken together, our work demonstrated that overexpression of the ZmRAFS gene in maize, in contrast to Arabidopsis, increased the raffinose content in leaves, assisted the leaf to retain water, and enhanced the plant drought stress tolerance without causing a detectable growth penalty. Significance Statement Raffinose has been positively correlated with drought tolerance but its mechanism of action remains obscure. The amounts of raffinose increased in leaves of maize plants constitutively overexpressing its RAFFINOSE SYNTHASE gene, which then assisted the leaf to retain water, and enhanced the plant drought stress tolerance without a growth penalty. 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A.</au><au>Downie, A. Bruce</au><au>Zhao, Tianyong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Raffinose positively regulates maize drought tolerance by reducing leaf transpiration</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2023-04</date><risdate>2023</risdate><volume>114</volume><issue>1</issue><spage>55</spage><epage>67</epage><pages>55-67</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY Drought stress is one of the major constraints of global crop production. Raffinose, a non‐reducing trisaccharide, has been considered to regulate positively the plant drought stress tolerance; however, evidence that augmenting raffinose production in leaves results in enhanced plant drought stress tolerance is lacking. The biochemical mechanism through which raffinose might act to mitigate plant drought stress remains unidentified. ZmRAFS encodes Zea mays RAFFINOSE SYNTHASE, a key enzyme that transfers galactose from the galactoside galactinol to sucrose for raffinose production. Overexpression of ZmRAFS in maize increased the RAFS protein and the raffinose content and decreased the water loss of leaves and enhanced plant drought stress tolerance. The biomass of the ZmRAFS overexpressing plants was similar to that of non‐transgenic control plants when grown under optimal conditions, but was significantly greater than that of non‐transgenic plants when grown under drought stress conditions. In contrast, the percentage of water loss of the detached leaves from two independent zmrafs mutant lines, incapable of synthesizing raffinose, was greater than that from null segregant controls and this phenomenon was partially rescued by supplementation of raffinose to detached zmrafs leaves. In addition, while there were differences in water loss among different maize lines, there was no difference in stomata density or aperture. Taken together, our work demonstrated that overexpression of the ZmRAFS gene in maize, in contrast to Arabidopsis, increased the raffinose content in leaves, assisted the leaf to retain water, and enhanced the plant drought stress tolerance without causing a detectable growth penalty. Significance Statement Raffinose has been positively correlated with drought tolerance but its mechanism of action remains obscure. The amounts of raffinose increased in leaves of maize plants constitutively overexpressing its RAFFINOSE SYNTHASE gene, which then assisted the leaf to retain water, and enhanced the plant drought stress tolerance without a growth penalty. 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subjects Arabidopsis - metabolism
carbohydrate metabolism
Corn
Crop production
Drought Resistance
drought stress
Droughts
Galactose
Galactosides
Gene Expression Regulation, Plant
Leaves
maize (Zea mays)
Oligosaccharides
Plant Leaves - genetics
Plant Leaves - metabolism
Plants
Plants (botany)
Plants, Genetically Modified - metabolism
Raffinose
RAFFINOSE SYNTHASE
Stomata
Stress, Physiological - genetics
Sucrose
Transgenic plants
Transpiration
Water - metabolism
Water loss
Zea mays
Zea mays - metabolism
title Raffinose positively regulates maize drought tolerance by reducing leaf transpiration
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