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Overexpression of Oscasp1 Improves Calcium Tolerance in Rice

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Overexpression of Oscasp1 Improves Calcium Tolerance in Rice International Journal of Molecular Sciences Article Overexpression of OsCASP1 Improves Calcium Tolerance in Rice Zhigang Wang †, Zhiwei Chen †, Xiang Zhang †, Qiuxing Wei, Yafeng Xin, Baolei Zhang, Fuhang Liu and Jixing Xia * State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Science and Technology, Guangxi University, Nanning 530004, China; [email protected] (Z.W.); [email protected] (Z.C.); [email protected] (X.Z.); [email protected] (Q.W.); [email protected] (Y.X.); [email protected] (B.Z.); [email protected] (F.L.) * Correspondence: [email protected]; Tel.: +86-0771-3236616 † These authors contributed equally to this work. Abstract: The Casparian strip domain protein 1 (OsCASP1) is necessary for the formation of the Casparian strip (CS) in the rice endodermis. It also controls Ca2+ transport to the stele. Here, we demonstrated that OsCASP1 overexpression enhanced Ca tolerance in rice. Under normal conditions, OsCASP1-overexpressed lines showed similar concentrations of essential metals in the roots and shoots compared to the wild type, while under high Ca conditions, Ca in the roots, shoots, and xylem sap of the OsCASP1-overexpressed lines was significantly decreased. This did not apply to other essential metals. Ca-inhibited growth was significantly alleviated in the OsCASP1-overexpressed lines. Furthermore, OsCASP1 overexpression resulted in earlier formation of both the CS and functional apoplastic barrier in the endodermis but did not induce ectopic CS formation in non- endodermal cell layers and affect suberin accumulation in the endodermis. These results indicate that the overexpression of OsCASP1 promotes CS formation in endodermal cells and inhibits Ca2+ Citation: Wang, Z.; Chen, Z.; Zhang, transport by the apoplastic pathway, restricting Ca accumulation in the roots and shoots under high X.; Wei, Q.; Xin, Y.; Zhang, B.; Liu, F.; Ca conditions. Taken together, the results suggest that OsCASP1 overexpression is an effective way Xia, J. Overexpression of OsCASP1 to improve rice adaptation to high Ca environments. Improves Calcium Tolerance in Rice. Int. J. Mol. Sci. 2021, 22, 6002. Keywords: Casparian strip; suberin lamellae; apoplastic barrier; calcium; lignin https://doi.org/10.3390/ijms22116002 Academic Editor: Marcello Iriti 1. Introduction Received: 13 April 2021 Calcium (Ca) is one of the most abundant metal elements in soil, which normally Accepted: 30 May 2021 contains large amounts of exchangeable Ca (300–5000 ppm) [1]. It is an essential macronu- Published: 1 June 2021 trient for plant growth and is involved in many biological processes, including cell division and expansion, structural integrity, and cellular signaling [2–6]. However, high cytosolic Publisher’s Note: MDPI stays neutral Ca2+ concentrations are cytotoxic [7,8]. Excessive Ca2+ restricts plant growth in calcare- with regard to jurisdictional claims in ous soils [7]. Therefore, optimal Ca concentrations are required for normal plant growth published maps and institutional affil- and development. iations. Divalent cation Ca2+ in the soil solution are taken up by the root system and radially delivered to the xylem by apoplastic and symplastic pathways [9–11]. In roots, two en- dodermal barriers, Casparian strip (CS) and suberin lamellae, are considered to limit the apoplastic flow of Ca across the endodermis into the xylem. These two barriers develop Copyright: © 2021 by the authors. gradually during the root differentiation [12,13]. At the primary developmental stage of Licensee MDPI, Basel, Switzerland. endodermis, CS formation is initiated at a few millimeters from the root apex. After the CS This article is an open access article formation and maturation in the root differentiation zone, suberin lamellae are deposited distributed under the terms and between the primary cell wall and the plasma membrane surrounding endodermal cells. conditions of the Creative Commons Attribution (CC BY) license (https:// When the CS located in the anticlinal cell wall between endodermal cells is completely 2+ creativecommons.org/licenses/by/ formed, transport of Ca to the xylem must use a symplastic pathway. In this case, the 2+ 4.0/). apoplastic Ca diffuses into the cytoplasm of the endodermal cells through Ca channels Int. J. Mol. Sci. 2021, 22, 6002. https://doi.org/10.3390/ijms22116002 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 6002 2 of 11 Int. J. Mol. Sci. 2021, 22, 6002 2 of 11 the apoplastic Ca2+ diffuses into the cytoplasm of the endodermal cells through Ca chan- nels in the plasma membrane [10]. Subsequently, Ca2+ is exported from the symplast of in the plasmathe membrane endodermal [10]. cells Subsequently, into the stele Ca 2+by isCa exported2+ transporters from thesuch symplast as Ca2+-ATPases of the [10]. When endodermal cellssuberin into lamellae the stele cover by Ca the2+ endodermaltransporters cells, such direct as Ca Ca2+-ATPases2+ uptake from [10]. the When apoplast into the suberin lamellaeendodermis cover the endodermalis prevented, cells, and the direct Ca Ca2+ must2+ uptake be taken from up the into apoplast the symplast into the from the outer endodermis iscell prevented, layers [10]. and However, the Ca2+ must the precise be taken roles up of into these the two symplast endodermal from the barriers outer in regulating cell layers [10].Ca However,2+ transport the into precise the xylem roles of for these transfer two endodermalto the shoot are barriers poorly in understood. regulating Ca2+ transport intoInterestingly, the xylem for in transfer Arabidopsis to the, several shoot areCS poorlymutants understood. such as casp1, casp3, esb1, myb36, and Interestingly,lotr1 indisplayedArabidopsis similar, several shoot CS ionomic mutants alterations, such as casp1, including casp3, esb1 low, myb36Ca accumulation, and [14–16]. lotr1 displayedIt similarwas proposed shoot ionomic that an alterations, increase inincluding endodermal low suberization Ca accumulation in these [14 –mutants16]. inhibited It was proposedCa2+ that transport an increase into the in endodermal xylem by the suberization symplastic pathway, in these mutants leading inhibitedto the reduced Ca con- Ca2+ transportcentration into the in xylem the shoots by the [15,16]. symplastic Rice differs pathway, from leading Arabidopsis to the in reducedhaving two Ca CSs in the ex- concentrationodermis in the shoots and endodermis, [15,16]. Rice differsrespectively from Arabidopsis[17]. Apoplasticin having Ca2+ twouptake CSs may in the occur largely in exodermis andthe endodermis, root tip where respectively the CS is [ 17formed]. Apoplastic in the endodermis Ca2+ uptake but may not occur the exodermis largely in [18]. A recent the root tip wherereport the shows CS is formedthat OsCASP1 in the endodermis is only involved but not in theCS formation exodermis in [18 the]. A root recent endodermis [18]. report shows thatIn oscasp1OsCASP1, defectiveis only endodermal involved in CSCS formationformation inresulted the root in endodermis uncontrolled [18 apoplastic]. Ca2+ In oscasp1, defectivetransport endodermal to the stele, CS which formation is prevented resulted by in th uncontrollede CS in the wild apoplastic type, resulting Ca2+ in the over- transport to theaccumulation stele, which of isCa prevented in the shoot by [18]. the CSTherefore, in the wildthe role type, of resultingthe CS in controlling in the Ca accu- over-accumulationmulation of Ca in inshoots the shoot differs [18 between]. Therefore, Arabidopsis the role and of therice. CS in controlling Ca accumulation in shootsTo further differs investigate between Arabidopsis the role ofand OsCASP1 rice. in rice CS formation and Ca uptake, in To furtherthis investigate study, we the generated role of OsCASP1 OsCASP1in overexpression rice CS formation transgenic and Ca uptake,lines and in characterized this study, wethem. generated We foundOsCASP1 thatoverexpression OsCASP1 overexpression transgenic lines induced andcharacterized early formation them. of the CS in the We found thatrootOsCASP1 tip andoverexpression selectively reduced induced Ca early accumula formationtion in of the CSroot in and the rootshoot tip under high Ca and selectivelyconditions. reduced Ca Furthermore, accumulation the in overexpre the root andssion shoot lines under enhanced high rice Ca conditions. tolerance to excess Ca. Furthermore,This the overexpressionwork enriches our lines understanding enhanced rice of tolerancethe interrelationships to excess Ca. between This work CS formation, Ca enriches our understandinguptake, and Ca oftolerance the interrelationships in rice. between CS formation, Ca uptake, and Ca tolerance in rice. 2. Results 2. Results 2.1. Expression2.1. of OsCASP1 Expression in of Transgenic OsCASP1 Lines in Transgenic Lines OsCASP1 wasOsCASP1 overexpressed was overexpressed in rice plants underin rice theplants control under of the maizecontrol ubiquitin of the maize ubiquitin promoter. Twopromoter. independent Two transgenic independent lines transgenic (pOX-1 and lines pOX-2) (pOX-1 were and produced pOX-2) were for subse- produced for sub- quent experiments.sequent RT-qPCR experiments. analysis RT-qPCR showed anal significantlyysis showed higher significantlyOsCASP1 higherexpression OsCASP1 expression in both the rootsin both and the shoots roots of and the twoshoots transgenic of the two lines transg thanenic in thelines wild-type than in the rice wild-type (WT) rice (WT) (Figure1A), ranging(Figure from 1A), a ranging
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