plants-12-02136-v2.pdf

Citation:Reguera,M.;Camacho-Cristbal,J.J.Molecular,Metabolic and PhysiologicalResponses to Boron Stress in HigherPlants.Plants 2023,12,2136.https:/doi.org/10.3390/plants12112136Received:16 May 2023Accepted:24 May 2023Published:28 May 2023Copyright:2023 by the authors.Licensee MDPI,Basel,Switzerland.This article is an open access articledistributedunderthetermsandconditions of the Creative CommonsAttribution(CC BY)license(https:/creativecommons.org/licenses/by/4.0/).plantsEditorialMolecular,Metabolic and Physiological Responses to BoronStress in Higher PlantsMara Reguera1,*,and Juan Jos Camacho-Cristbal2,*,1Departamento de Biologa,Universidad Autnoma de Madrid,c/Darwin 2,Campus de Cantoblanco,28049 Madrid,Spain2Departamento de Fisiologa,Anatoma y Biologa Celular,Facultad de Ciencias Experimentales,Universidad Pablo de Olavide,41013 Sevilla,Spain*Correspondence:maria.reguerauam.es(M.R.);jjcamcriupo.es(J.J.C.-C.)These authors contributed equally to this work.1.BackgroundAlthoughtheessentialityofboron(B)forplantgrowthhasrecentlybeenquestioned1,raising an exciting discussion between“Boronists”2,3,its requirement in plant develop-ment was first established at the beginning of the 20th century 4.B,as boric acid(H3BO3)and tetrahydroxyl borate anion B(OH)4,can form complexes with biological compoundscontaining two hydroxyl groups in cis-configuration.In this regard,it has been proposedthat the binding capacity of B plays a key role in biological systems by stabilizing moleculeswith cis-diol groups,regardless of the role played by these molecules 5.Nonetheless,todate,the only evidence for a direct involvement of B in plant metabolism comes from itsstructural role in the cell wall through the formation of ester bonds between the borateanion and the apiose residues of two molecules of rhamnogalacturonan II(RGII)6,7.However,this evidence cannot explain the plethora of plant processes affected by bothB deficiency and toxicity,so the possibility that other primary functions of B may existshould not be ruled out.Furthermore,it should be noted that B is an essential element forvascular plants that have a very narrow range of optimal concentrations,so controlling itsavailability to plants in soils and irrigation water is crucial for agricultural production.Infact,both B deficiency and toxicity have negative effects on the development and yield ofcrop plants 810.Therefore,knowledge of the molecular,metabolic,and physiological changes inducedby B deficiency or toxicity,as well as the characterization of the signaling pathways forthese responses,which has advanced greatly in recent years,can contribute not only to abetter understanding of the role of B in plants,but can also provide efficient strategies toimprove B stress tolerance in plants.In line with this,this Special Issue of Plants presentsa collection of eight manuscripts covering basic and applied topics on the response ofvascular plants to B stress.2.Main Findings Considered in this Special Issue2.1.One-Time Foliar Application and Continuous Resupply via Roots Equally Improved theGrowth and Physiological Response of B-Deficient Oilseed Rape 11B deficiency problems usually occur in regions with high rainfall conditions whereboric acid in the soil solution can easily leach out.The symptoms of B deficiency in cropplants cultivated on B-deficient soils can be alleviated by the application of B fertilizers,assoil fertilization or foliar spray.In this regard,Dinh et al.11 have studied the effectivenessof B resupply via roots and leaves to alleviate several symptoms of B deficiency in oilseedrape(Brassica napus L.)plants grown hydroponically.They concluded that both types ofB fertilization to oilseed rape plants can partially resolve the effects of B deficiency ondry matter production,net photosynthesis,and sugar contents,and on the expression ofspecific B transporters.Plants 2023,12,2136.https:/doi.org/10.3390/plants12112136https:/ 2023,12,21362 of 42.2.Crosstalk of Cytokinin with Ethylene and Auxin for Cell Elongation Inhibition and BoronTransport in Arabidopsis Primary Root under Boron Deficiency 12The knowledge on the signaling pathways for the response of plants to B deficiency hasadvanced greatly in recent years.For instance,recent studies revealed the involvement ofhormones(including ethylene,auxin,cytokinin,brassinosteroids,and ABA),calcium,andreactive oxygen species in the orchestrated signaling pathways of B stress responses 13.Findings in these fields can contribute not only to a better understanding of the role of Bin plants,but also provide efficient strategies to improve B stress tolerance in plants.Inthis regard,Herrera-Rodrguez et al.12 provided evidence that cytokinins negativelyregulate root cell elongation in Arabidopsis plants subjected to B deficiency through twoindependent pathways involving ethylene and auxins.The results also suggest that thesephytohormones regulate the gene expression of several B transporters in the root.2.3.Salt-Pretreatment-Mediated Alleviation of Boron Toxicity in Safflower Cultivars:Growth,Boron Accumulation,Photochemical Activities,and Antioxidant Defense Response 14B toxicity and salinity stresses often occur together,so there is growing interest instudying the interactive effects of these stresses on plant growth 15.The work of Ar-slan et al.14 analyzed the potential use of salt pretreatment to alleviate the effects ofB toxicity on growth,phytoremediation capacity,photosynthesis,and oxidative stress intwo safflower cultivars(Carthamus tinctorius L.).Results suggested that salt pretreatmentpartially mitigated several of the biochemical and physiological changes caused by Btoxicity.2.4.Carbon-11 Radiotracing Reveals Physiological and Metabolic Responses of Maize Grown underDifferent Regimes of Boron Treatment 16B deficiency can alter plant growth and physiology,which has been related to itsrole in stabilizing cell wall structure 17.In this sense,monocots have generally showna lower B requirement,which has been linked to a reduced pectin content comparedto dicotyledonous plants.However,positive responses in terms of plant productivityhave been reported in different cereal species,including maize 18.In the work per-formed by Wilder et al.16,the impact of B on carbon partitioning was evaluated using11C-radiotracing,highlighting the strong effect of B deficiency on metabolism.Furthermore,they demonstrated that synergistic and antagonistic relations occur among certain mineralnutrients when changing B supply.2.5.Citrus Physiological and Molecular Response to Boron Stresses 19B is an essential element for vascular plants that has a very narrow range of optimalconcentrations,so controlling its availability to plants in soils and irrigation water is crucialfor agricultural production.In fact,both B deficiency and toxicity have negative effectson the development and yield of crop plants 810.In this regard,the essentiality of B incitrus plants was discovered soon after B was shown to be essential for plants 4,20,andsince then different works have described the effects of B deficiency or toxicity in theseplant species.Yang et al.19 reviews the research performed in Citrus when subjected to Bstress,and emphasizes the importance of further analyzing B transport and allocation inCitrus,a genus that comprises important crops for the fruit industry.2.6.Silicon Differently Affects the Apoplastic Binding of Excess Boron in Wheat andSunflower Leaves 21B toxicity problems often occur in crops of arid/semiarid regions with low rainfall andhigh water evaporation where B accumulates in the uppermost layers of the soil,reachingtoxic levels for plants.Alleviating the symptoms of B toxicity in crop plants can be achievedby applying elements that have a positive impact on the physiological tolerance of plants(i.e.,those preventing oxidative stress).For instance,Savic et al.21 demonstrated thatSi fertilization significantly decreased B concentration in wheat(Triticum vulgare L.)andsunflower(Helianthus annuus L.)leaves when growing under high-B conditions,leading toPlants 2023,12,21363 of 4a recovery of plant growth,especially in wheat.Interestingly,Si application increased theB-binding capacity of the leaf apoplast in wheat but not in sunflower.2.7.Response of Maize(Zea mays L.)to Drought under Salinity and Boron Stress in theAtacama Desert 22Drought can interfere with B influx as it limits water transpiration and uptake 23.Onthe other hand,interactions between salinity and B stress(that could act simultaneously,especially in arid and semiarid regions 24)have been described in different plant speciesand linked to limited water uptake 25.The work of Riveros-Burgos et al.22 evaluatedthe effect of the combination of the three stressors(drought,salinity,and high B)on thephysiological response of lluteo maize(Zea mays L.),which is adapted to the AtacamaDesert,pointing to a genotypic-dependent response in maize to the simultaneous action ofthese environmental stresses.2.8.What Can Boron Deficiency Symptoms Tell Us about Its Function and Regulation?26B-deficient plants may exhibit a wide range of symptoms depending on the species andthe developmental stage of the plant 27.In recent years,the use of novel molecular toolshas allowed for the discovery of novel functions and ligands of B in organisms includingbacteria,animals,and plants.Still,there is a general lack of knowledge regarding thespecific functions of B,B stress signaling pathways,and B interactors beyond its structuralrole in the plant cell wall.Bolaos et al.26 proposed a model integrating B-deficiencysymptoms and signaling pathways,summarizing the current knowledge regarding Bputative ligands in plants.Author Contributions:M.R.and J.J.C.-C.contributed equally to the preparation of this Editorial.Allauthors have read and agreed to the published version of the manuscript.Funding:The authors gratefully acknowledge the financial support received from the Ministerio deCienciaeInnovacin(MICINN,Spain)andtheAgenciaEstataldeInvestigacin(PID2020-118327GB-I00).Data Availability Statement:Data sharing not applicable.Acknowledgments:We specially thank all the authors that have contributed to this Special Issue andthe Section Managing Editor,who has greatly helped us throughout the editorial process.Conflicts of Interest:The author declares no conflict of interest.References1.Lewis,D.H.Boron:The essential element for vascular plants that never was.New Phytol.2019,221,16851690.CrossRef2.Gonzlez-Fontes,A.Why boron is an essential element for vascular plants.New Phytol.2020,226,12281230.CrossRef3.Wimmer,M.A.;Abreu,I.;Bell,R.W.;Bienert,M.D.;Brown,P.H.;Dell,B.;Fujiwara,T.;Goldbach,H.E.;Lehto,T.;Mock,H.P.;et al.Boron:An essential element for vascular plants.New Phytol.2020,226,12321237.CrossRef4.Warington,K.The effect of boric acid and borax on the broad bean and certain other plants.Ann.Bot.1923,37,629672.CrossRef5.Bolaos,L.;Lukaszewski,K.;Bonilla,I.;Blevins,D.Why Boron?Plant Physiol.Biochem.2004,42,907912.CrossRef PubMed6.Kobayashi,M.;Matoh,T.;Azuma,J.Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higherplant cell walls.Plant Physiol.1996,110,10171020.CrossRef PubMed7.ONeill,M.A.;Warrenfeltz,D.;Kates,K.;Pellerin,P.;Doco,T.;Darvill,A.G.;Albersheim,P.Rhamnogalacturonan-II,a pecticpolysaccharide in the walls of growing plant cell,forms a dimer that is covalently cross-linked by a borate ester.J.Biol.Chem.1996,271,2292322930.CrossRef8.Goldbach,H.E.;Wimmer,M.A.Boron in Plants and Animals:Is There a Role beyond Cell-Wall Structure?J.Plant Nutr.Soil Sci.2007,170,3948.CrossRef9.Landi,M.;Margaritopoulou,T.;Papadakis,I.E.;Araniti,F.Boron toxicity in higher plants:An update.Planta2019,250,10111032.CrossRef PubMed10.Brdar-Jokanovic,M.Boron toxicity and deficiency in agricultural plants.Int.J.Mol.Sci.2020,21,1424.CrossRef11.Dinh,A.Q.;Naeem,A.;Sagervanshi,A.;Mhling,K.H.One-Time Foliar Application and Continuous Resupply via Roots EquallyImproved the Growth and Physiological Response of B-Deficient Oilseed Rape.Plants 2021,10,866.CrossRef12.Herrera-Rodrguez,M.B.;Camacho-Cristbal,J.J.;Barrero-Rodrguez,R.;Rexach,J.;Navarro-Gochicoa,M.T.;Gonzlez-Fontes,A.Crosstalk of Cytokinin with Ethylene and Auxin for Cell Elongation Inhibition and Boron Transport in Arabidopsis Primary Rootunder Boron Deficiency.Plants 2022,11,2344.CrossRef PubMedPlants 2023,12,21364 of 413.Chen,X.;Smith,S.M.;Shabala,S.;Yu,M.Phytohormones in plant responses to boron deficiency and toxicity.J.Exp.Bot.2023,74,743754.CrossRef PubMed14.Arslan,.;ulha Erdal,S.;Ekmeki,Y.Salt Pretreatment-Mediated Alleviation of Boron Toxicity in Safflower Cultivars:Growth,Boron Accumulation,Photochemical Activities,Antioxidant Defense Response.Plants 2022,11,2316.CrossRef15.Pandey,A.;Khan,M.K.;Hakki,E.E.;Gezgin,S.;Hamurcu,M.Combined Boron Toxicity and Salinity StressAn Insight into ItsInteraction in Plants.Plants 2019,8,364.CrossRef16.Wilder,S.L.;Scott,S.;Waller,S.;Powell,A.;Benoit,M.;Guthrie,J.M.;Schueller,M.J.;Awale,P.;McSteen,P.;Matthes,M.S.;et al.Carbon-11 Radiotracing Reveals Physiological and Metabolic Responses of Maize Grown under Different Regimes of BoronTreatment.Plants 2022,11,241.CrossRef17.Goldbach,H.E.;Huang,L.;Wimmer,M.A.Boron Functions in Plants and Animals:Recent Advances in Boron Research andOpen Questions.In Advances in Plant and Animal Boron Nutrition;Xu,F.,Goldbach,H.,Brown,P.,Bell,R.,Fujiwara,T.,Hunt,C.,Goldberg,S.,Shi,L.,Eds.;Springer:Dordrecht,The Netherlands,2007;pp.325.CrossRef18.Lordkaew,S.;Dell,B.;Jamjod,S.;Rerkasem,B.Boron deficiency in maize.Plant Soil 2011,342,207220.CrossRef19.Yang,L.-T.;Pan,J.-F.;Hu,N.-J.;Chen,H.-H.;Jiang,H.-X.;Lu,Y.-B.;Chen,L.-S.Citrus Physiological and Molecular Response toBoron Stresses.Plants 2022,11,40.CrossRef20.Haas,A.R.C.Boron as an essential element for healthy growth of citrus.Bot.Gaz.1930,89,410413.CrossRef21.Savic,J.;Pavlovic,J.;Stanojevic,M.;Bosnic,P.;Kostic Kravljanac,L.;Nikolic,N.;Nikolic,M.Silicon Differently Affects ApoplasticBinding of Excess Boron in Wheat and Sunflower Leaves.Plants 2023,12,1660.CrossRef22.Riveros-Burgos,C.;Bustos-Pea,R.;Esteban-Condori,W.;Bastas,E.Response of Maize(Zea mays L.)to Drought under Salinityand Boron Stress in the Atacama Desert.Plants 2023,12,1519.CrossRef23.Aydin,M.;Tombuloglu,G.;Sakcali,M.S.;Hakeem,K.R.;Tombuloglu,H.Boron Alleviates Drought Stress by Enhancing GeneExpression and Antioxidant Enzyme Activity.J.Soil Sci.Plant Nutr.2019,19,545555.CrossRef24.Gupta,E.C.;Jame,Y.W.;Campbell,C.A.;Leyshon,A.J.;Nicholaichuk,W.Boron toxicity and deficiency:A review.Can.J.Soil Sci.1985,65,381409.CrossRef25.Martnez-Ballesta,M.;Bastas,E.;Zhu,C.;Schffner,A.R.;Gonzlez-Moro,B.;Gonzlez-Murua,C.;Carvajal,M.Boric acid andsalinity effects on maize roots.Response of aquaporins ZmPIP1 and ZmPIP2,and plasma membrane H+-ATPase,in relation towater and nutrient uptake.Physiol.Plant.2008,132,479490.CrossRef26.Bolaos,L.;Abreu,I.;Bonilla,I.;Camacho-Cristbal,J.J.;Reguera,M.What Can Boron De