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Differential response of Trichloris ecotypes from different habitats to drought and salt stress

Abstract

Native plant genetic resources have evolved from long processes of natural selection and adaptation to specific environments, and have developed tolerance to various stresses prevailing in their natural habitats via adaptive morphophysiological features. The associations between environmental stress conditions (aridity degree and salinity) prevailing in the original habitat of Argentine native Trichloris species (T. crinita and T. pluriflora) and various biometric and physiological traits were evaluated. Trials were carried out in hydroponics in a growth chamber. Components of initial plant growth, oxidative stress expression and antioxidant activity under drought and salt stress were measured in ecotypes of both species, as well as Na+ and K+ leaf tissue concentration and excretion rates under salinity. Ecotypes from arid and semiarid origin of both species had higher drought tolerance. Regarding salt stress, T. crinita ecotype from alkali soil showed stimulated growth under salinity and an ecotype from saline soil kept high root and shoot biomass production. Although the ecotypes of T. pluriflora were not significantly salt-sensitive, none stood out. Many active salt glands on the abaxial leaf surface, high Na/K excretion ratio and high leaf tissue concentration of sodium were found for salt-tolerant ecotypes. This study identified ecotypes with tolerance to prevailing stressful conditions of natural habitat of native forage species to be introduced to plant breeding programmes for restorations purposes. Trichloris pluriflora is an unexplored genetic resource for semiarid rangeland, thus this study is the first report of drought tolerant ecotypes.

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References

  • Abrol IP, Yadav JS, Massoud FI (1988) Salt-affected soils and their management. Food and Agriculture Organization Soils Bulletin N° 39, Rome, Italy

  • Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR et al (2000) The evolution of plant ecophysiological traits: recent advances and future directions new research addresses natural selection, genetic constraints, and the adaptive evolution of plant ecophysiological traits. Bioscience 50(11):979–995

    Google Scholar 

  • Adedapo AA, Jimoh FO, Afolayan AJ, Masika PJ (2009) Antioxidant properties of the methanol extracts of the leaves and stems of Celtis africana. Rec Nat Prod 3:23–31

    CAS  Google Scholar 

  • Allard RW, Jain SK, Workman PL (1968) The genetics of inbreeding populations. Adv Genet 14:55–131

    Google Scholar 

  • Aronson J (1985) Economic Halophytes. A global review. In: Wickens GE, Gooding JR, Field DV (eds) Plants for arid lands. Allen and Unwin, London, pp 177–188

    Google Scholar 

  • Bal AR, Dutt SK (1986) Mechanism of salt tolerance in wild rice (Porteresia coarctata Roxb.). Plant Soil 92(3):399–404

    CAS  Google Scholar 

  • Begg JE, Turner NC (1976) Crop water deficits. Adv Agron 28:161–217

    CAS  Google Scholar 

  • Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76

    CAS  PubMed  Google Scholar 

  • Bergendi L, Benes L, Durackova Z, Ferenik M (1999) Chemistry, physiology and pathology of free radicals. Life Sci 65:1865–1874

    CAS  PubMed  Google Scholar 

  • Bischoff A, Crémieux L, Smilauerova M, Lawson CS, Mortimer SR, Dolezal J et al (2006) Detecting local adaptation in widespread grassland species—the importance of scale and local plant community. J Ecol 94(6):1130–1142

    Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    CAS  PubMed  Google Scholar 

  • Bradley St. Clair J, Kilkenny FF, Johnson RC, Shaw NL, Weaver G (2013) Genetic variation in adaptive traits and seed transfer zones for Pseudoroegneria spicata (bluebunch wheatgrass) in the northwestern United States. Evol Appl 6(6):933–948

    PubMed  PubMed Central  Google Scholar 

  • Bradshaw AD (1984) Ecological significance of geneticvariation between populations. In: Dirzo R, Sarukhan J (eds) Perspectives on plant population biology. Sinauer Associates, Sunderland, pp 213–228

    Google Scholar 

  • Chanda S, Dave R (2009) In vitro models for antioxidant activity evaluation and some medicinal plants possessing antioxidant properties: an overview. Afr J Microbiol Res 3(13):981–996

    Google Scholar 

  • Clayton WD, Renvoize SA (1986) Genera Graminum, grasses of the world. Kew bulletin additional series 13

  • Columbus JT, Cerros-Tlatilpa R, Kinney MS, Siqueiros-Delgado ME, Bell HL, Griffith MP, Refulio-Rodríguez NF (2007) Phylogenetics of Chloridoideae (Gramineae): a preliminary study based on nuclear ribosomal internal transcribed spacer and chloroplast trnL–F sequences. Aliso J Syst Evol Bot 23:565–579

    Google Scholar 

  • Couso LL, Fernández RJ (2012) Phenotypic plasticity as an index of drought tolerance in three Patagonian steppe grasses. Ann Bot 110(4):849–857

    CAS  PubMed  PubMed Central  Google Scholar 

  • Couso LL, Gatti ML, Cornaglia PS, Schrauf GE, Fernández RJ (2010) Are more productive varieties of Paspalum dilatatum less tolerant to drought? Grass Forage Sci 65(3):296–303

    Google Scholar 

  • de Luca M, García Seffino L, Grunberg K, Salgado M, Córdoba A, Luna C et al (2001) Physiological causes for decreased productivity under high salinity in Boma, a tetraploid Chloris gayana cultivar. Aust J Agric Res 52:903–910

    Google Scholar 

  • Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228

    CAS  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32(1):79–91

    CAS  Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini MG, González L, Tablada M, Robledo CW (2018) InfoStat versión 2018. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. https://www.InfoStat.com.ar

  • Endler JA (1986) Natural selection in the wild (No. 21). Princeton University Press, Princeton

    Google Scholar 

  • Falconer DS, Mackay TFC (2006) Introduction to quantitative genetics, 4th edn. Addison Wesley Longman Limited, Harlow

    Google Scholar 

  • Fernández OA, Busso CA (1997) Arid and semi-arid rangelands: two thirds of Argentina. RALA Rep 200:41–60

    Google Scholar 

  • Fernández RJ, Reynolds JF (2000) Potential growth and drought tolerance of eight desert grasses: lack of a trade-off? Oecologia 123:90–98

    PubMed  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179(4):945–963

    CAS  PubMed  Google Scholar 

  • Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115(3):327–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flowers TJ, Flowers SA (2005) Why does salinity pose such a difficult problem for plant breeders? Agric Water Manage 78:15–24

    Google Scholar 

  • Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37(7):604–612

    Google Scholar 

  • Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115(3):419–431

    CAS  PubMed  Google Scholar 

  • Foulkes MJ, Hawkesford MJ, Barraclough PB, Holdsworth MJ, Kerr S, Kightley S, Shewry PR (2009) Identifying traits to improve the nitrogen economy of wheat: recent advances and future prospects. Field Crops Res 114(3):329–342

    Google Scholar 

  • Gastal F, Durand JL (2000) Effects of nitrogen and water supply on N and C and partitioning in defoliated swards. In: Lemaire G, Hodgson J, de Moraes A, de Carvalho PC, Nabinger C (eds) Grassland ecophysiology and grazing ecology. CABI Publishing, Wallingford, pp 15–39

    Google Scholar 

  • González CL, Dodd JD (1979) Production responses of native and introduced grasses to mechanical brush manipulation, seeding, and fertilization. J Range Manag 32:305–309

    Google Scholar 

  • González-Paleo L, Ravetta DA (2011) Indirect changes associated with a selection program for increased seed-yield in wild species of Lesquerella (Brassicaceae): Are we developing a phenotype opposite to the expected ideotype? Ind Crops Prod 34(2):1372–1380

    Google Scholar 

  • Greco SA, Cavagnaro JB (2002) Effect of drought in biomass production and allocation in three varieties of Trichloris crinita (Poaceae) a forage grass from the arid Monte region of Argentina. Plant Ecol 64:125–135

    Google Scholar 

  • Greco SA, Cavagnaro JB (2005) Growth characteristics associated with biomass production in three varieties of Trichloris crinita (Poaceae), a forage grass native to the arid regions of Argentina. Rangeland J 27(2):135–142

    Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31(1):149–190

    CAS  Google Scholar 

  • Gutiérrez HF, Richard GA, Cerino MC, Pensiero JF (2016) Sistema reproductivo de Trichloris (Poaceae: Chloridoideae, Chlorideae). Boletín de la Sociedad Argentina de Botánica 51(1):111–122

    Google Scholar 

  • Harlan JR (1976) Genetic resources in wild relatives of crops. Crop Sci 16:329–332

    Google Scholar 

  • Hediye Sekmen A, Türkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant 131(3):399–411

    Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347.

  • Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207(4):604–611

    CAS  Google Scholar 

  • Hsiao TC, Acevedo E (1974) Plant responses to water deficits, water-use efficiency, and drought resistance. Agric Meteorol 14(1–2):59–84

    Google Scholar 

  • Jeschke WD, Pate JS (1991) Cation and chloride partitioning through xylem and phloem within the whole plant of Ricinus communis L. under conditions of salt stress. J Exp Bot 42(9):1105–1116

    CAS  Google Scholar 

  • Jeschke WD, Aslam Z, Greenway H (1986) Effects of NaCl on ion relations and carbohydrate status of roots and on osmotic regulation of roots and shoots of Atriplex amnicola. Plant Cell Environ 9:559–569

    CAS  Google Scholar 

  • Joshi J, Schmid B, Caldeira MC, Dimitrakopoulos PG, Good J, Harris R, Hector A, Huss-Danell K, Jumpponen A, Minns A, Mulder CPH, Pereira JS, Prinz A, Scherer-Lorenzen M, Siamantziouras A-SD, Terry AC, Troumbis AY, Lawton JH (2001) Local adaptation enhances performance of common plant species. Ecol Lett 4:536–544

    Google Scholar 

  • Kobayashi H (2008) Ion secretion via salt glands in Poaceae. Jpn J Plant Sci 2:1–8

    Google Scholar 

  • Kobayashi H, Masaoka Y, Takahashi Y, Ide Y, Sato S (2007) Ability of salt glands in Rhodes grass (Chloris gayana Kunth) to secrete Na+ and K+. Soil Sci Plant Nutr 53(6):764–771

    CAS  Google Scholar 

  • Kozub PC, Barboza K, Galdeano F, Quarin CL, Cavagnaro JB, Cavagnaro PF (2017) Reproductive biology of the native forage grass Trichloris crinita (Poaceae, Chloridoideae). Plant Biol 19:444–453

    CAS  PubMed  Google Scholar 

  • Lavado R (2008) Visión sinteetica de la distribución y magnitud de los suelos afectados por salinidad en la Argentina. In: Taleisnik E, Grunberg K, Santa María G (eds) La salinización de suelos en la Argentina: su impacto en la producción agropecuaria. EDUCC, Córdoba, pp 11–15

    Google Scholar 

  • Liphschitz N, Waisel Y (1974) Existence of salt glands in various genera of the Gramineae. New Phytol 73:507–513

    Google Scholar 

  • Liu L, Sun Y, Laura T, Liang X, Ye H, Zeng X (2009) Determination of polyphenolic content and antioxidant activity of Kudingcha made from Ilex kudingcha C.J Tseng. Food Chem 112:35–41

    CAS  Google Scholar 

  • Luna C, García-Seffino L, Arias C, Taleisnik E (2000) Oxidative stress indicators as selection tools for salt tolerance. Plant Breed 119(4):341–345

    CAS  Google Scholar 

  • Luna DF, Aguirre A, Pittaro G, Bustos D, Ciacci B, Taleisnik E (2016) Nutrient deficiency and hypoxia as constraints to Panicum coloratum growth in alkaline soils. Grass Forage Sci 72(4):640–653

    Google Scholar 

  • Marcum KB (1999) Salinity tolerance mechanisms of grasses in the subfamily Chloridoideae. Crop Sci 39:1153–1160

    Google Scholar 

  • Marcum KB (2008) Saline tolerance physiology in grasses. In: Khan MA, Weber DJ (eds) Ecophysiology of high salinity tolerant plants. Springer, Netherlands, pp 157–172

    Google Scholar 

  • Marcum KB, Murdoch CL (1994) Salinity tolerance mechanisms of six C4 turfgrasses. J Am Soc Hortic Sci 119:779–784

    CAS  Google Scholar 

  • Marcum KB, Anderson SJ, Engelke MC (1998) Salt gland ion secretion: a salinity tolerance mechanism among five zoysiagrass species. Crop Sci 38:806–810

    Google Scholar 

  • Marcum KB, Wess G, Ray DT, Engelke MC (2003) Zoysiagrass, salt glands, and salt tolerance. USGA Turfgrass Environ Res Online 2:1–6

    Google Scholar 

  • Marinoni L (2017) Variabilidad en el peso de semillas del género Trichloris (Poaceae) en Argentina y su efecto en la respuesta al estrés hídrico y salino. Doctoral Thesis, Facultad de Ciencias Agrarias, Universidad Nacional del Litoral, Santa Fe, Argentina.

  • Marinoni L, Bortoluzzi A, Parra-Quijano M, Zabala JM, Pensiero JF (2015) Evaluation and improvement of the ecogeographical representativeness of a collection of the genus Trichloris in Argentina. Genet Res Crop Evol 62:593–604

    Google Scholar 

  • Marinoni L, Zabala JM, Parra-Quijano M, Fernández RJ, Pensiero JF (2018) Genetic and environmental variation of seed weight in Trichloris species (Chloridoideae, Poaceae) and its association with seedling stress tolerance. Plant Ecol Div. https://doi.org/10.1080/17550874.2018.1449262

    Article  Google Scholar 

  • Mishra P, Bhoomika K, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250(1):3–19

    CAS  PubMed  Google Scholar 

  • Moussa HR, Abdel-Aziz SM (2008) Comparative response of drought tolerant and drought sensitive maize genotypes to water stress. Aust J Crop Sci 1(1):31–36

    Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    CAS  PubMed  Google Scholar 

  • Naz N, Hameed M, Wahid A, Arshad M, Ahmad A, Sajid M (2009) Patterns of ion excretion and survival in two stoloniferous arid zone grasses. Physiol Plant 135:185–195

    CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    CAS  Google Scholar 

  • Oi T, Sasagawa TM, Taniguchi M, Miyake H (2013) Growth and salt excretion via the salt glands of Rhodes grass in the soil damaged by the Tsunami. Jpn J Crop Sci 82:378–389

    CAS  Google Scholar 

  • Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defense in halophytes. Funct Plant Biol 40:832–847

    CAS  PubMed  Google Scholar 

  • Pensiero JF, Zabala JM, Marinoni L, Richard G (2017) Recursos fitogenéticos forrajeros nativos y naturalizados (RFNyN) para suelos salinos de la región chaqueña de Argentina. In: Taleisnik E, Lavado R (eds) La salinidad y alcalinidad en suelos de la Argentina y su efecto sobre vegetación natural y cultivos. Prospección y manejo para su aprovechamiento productivo, Orientación Gráfica Editora, Córdoba, Argentina, pp 373–419

    Google Scholar 

  • Peterson PM, Romaschenko K, Johnson G (2010) A classification of the Chloridoideae (Poaceae) based on multi-gene phylogenetic trees. Mol Phylogenet Evol 55:580–598

    CAS  PubMed  Google Scholar 

  • Quiroga E, Blanco L, Orionte E (2009) Evaluación de estrategias de rehabilitación de pastizales áridos. Ecol Austral 19:107–117

    Google Scholar 

  • Quiroga RE, Fernández RJ, Golluscio RA, Blanco LJ (2013) Differential water-use strategies and drought resistance in Trichloris crinita plants from contrasting aridity origins. Plant Ecol 214(8):1027–1035

    Google Scholar 

  • Ramadan T (2001) Dynamics of salt secretion by Sporobolus spicatus (Vahl) Kunth from sites of differing salinity. Ann Bot 87:259–266

    CAS  PubMed  Google Scholar 

  • Reynolds MP, Trethowan RM (2007) Physiological interventions in breeding for adaptation to abiotic stress. Frontis 121:27–144

    Google Scholar 

  • Reynolds JF, Smith DMS, Lambin EF, Turner BL, Mortimore M, Batterbury SP et al (2007) Global desertification: building a science for dryland development. Science 316(5826):847–851

    CAS  PubMed  Google Scholar 

  • Rozema J (1991) Growth, water and ion relationships of halophytic monocotyledonae and dicotyledonae; a unified concept. Aqua Bot 39:17–33

    Google Scholar 

  • Rúgolo ZE, Molina A (2012) Trichloris. In: Zuloaga FO, Rúgolo ZE, Anton AMR (eds) Flora vascular de la República Argentina. Vol. 3, Tomo 1. Monocotyledoneae. Aristidoidea a Pharoidea. 1 ed. Gráficamente Ediciones, Córdoba, Argentina, Poaceae, pp 167–169

  • Santamaria L, Figuerola J, Pilon JJ, Mjelde M, Green AJ, de Boer T, King RA, Gornall RJ (2003) Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology 84:2454–2461

    Google Scholar 

  • Scandalios JG (1993) Oxygen stress and superoxide dismutases. Plant Physiol 101:7–12

    CAS  PubMed  PubMed Central  Google Scholar 

  • Snow MD, Tingey DT (1985) Evaluation of a system for the imposition of plant water stress. Plant Physiol 77:602–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Yao J, Huang S, Long X, Wang J, Garcia-Garcia E (2009) Antioxidant activity of polyphenol and anthocyanin extracts from fruits of Kadsura coccinea (Lem.) AC. Smith Food Chem 117:276–281

    CAS  Google Scholar 

  • Tada Y, Komatsubara S, Kurusu T (2014) Growth and physiological adaptation of whole plants and cultured cells from a halophyte turf grass under salt stress. AoB Plants 6

  • Taleisnik EL, Anton AM (1988) Salt glands in Pappophorum (Poaceae). Ann Bot 62(4):383–388

    Google Scholar 

  • Taleisnik E, Peyrano G, Arias C (1997) Response of Chloris gayana cultivars to salinity. 1. Germination and early vegetative growth. Trop Grassl 31:232–240

    Google Scholar 

  • Thomson WW (1975) The structure and function of salt glands. In: Poljakoffmayber A, Gale J (eds) Plants in saline environments. Springer, Berlin, pp 118–148

    Google Scholar 

  • Venables AV, Wilkins DA (1978) Salt tolerance in pasture grasses. New Phytol 80(3):613–622

    CAS  Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83(2):278–282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol 12(1):188

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zabala JM, Delbino M, Giavedoni J, Pensiero J (2011) Glándulas de sal como criterio de selección y evaluación de la tolerancia a la salinidad en Trichloris crinita y Trichloris pluriflora. Segunda Reunión de la Red Argentina de Salinidad RASTUC 2011. Sociedad Rural de Tucumán, San Miguel de Tucumán, Argentina

  • Zhang HX, Yin LK, Pan BR (2003) A review on the study of salt glands of Tamarix. Acta Bot Boreal-Occident Sin 23:190–194

    Google Scholar 

  • Zhou S, Han JL, Zhao KF (2001) Advance of study on recretohalophytes. Chin J Appl Environ Biol 7:496–501

    CAS  Google Scholar 

Download references

Acknowledgements

Funding was provided by the CAI+D 2016 project of the Universidad Nacional del Litoral, and by the PICTO 2014 project “Native forage species for silvopastoral systems of the Argentinian Parque Chaqueño”, supported by the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT). Doctoral and postdoctoral studies of L.M. and G.A.R. were supported by scholarships granted by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

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Marinoni, L.R., Richard, G.A., Bustos, D. et al. Differential response of Trichloris ecotypes from different habitats to drought and salt stress. Theor. Exp. Plant Physiol. 32, 213–229 (2020). https://doi.org/10.1007/s40626-020-00182-x

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Keywords

  • Local adaptation
  • antioxidant activity
  • Oxidative stress
  • Salt glands
  • Trichloris crinita
  • Trichloris pluriflora