Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Abscisic acid and its metabolites are involved in drought tolerance in four native species of Patagonian semiarid shrublands (Argentina)

Ana M. Cenzano A C , Mariana Reginato B , M. Celeste Varela B and M. Virginia Luna B
+ Author Affiliations
- Author Affiliations

A Laboratorio de Ecofisiología y Bioquímica Vegetal, Instituto Patagónico para el Estudio de los Ecosistemas Continentales (IPEEC), Centro Científico Tecnológico Consejo Nacional de Investigaciones Científicas y Técnicas-Centro Nacional Patagónico (CCT CONICET-CENPAT), Boulevard Brown 2915. 9120, Puerto Madryn, Chubut, Argentina.

B Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto. Ruta 36, Km 601. 5800, Río Cuarto, Córdoba, Argentina.

C Corresponding author. Email: cenzano@cenpat-conicet.gob.ar

Australian Journal of Botany 66(8) 589-600 https://doi.org/10.1071/BT18049
Submitted: 09 March 2018  Accepted: 16 October 2018   Published: 3 December 2018

Abstract

Drought is the main stress that affects growth of native species of Patagonian Monte. Physiological and biochemical traits with functional roles in adaptation to drought are still scarce in native species. The aim of this study was to evaluate changes in dry matter content and abscisic acid (ABA) and its metabolites (phaseic acid-PA, dihydrophaseic acid-DPA, ABA conjugated with glucose-ABA-GE) level in green leaves and fine roots of four native species during contrasting seasons regarding water availability. Results show that grasses had higher leaf dry matter content (LDMC) and root dry matter content (RDMC) than Lycium chilense shrub and LDMC decreased during autumn in Larrea divaricata. In green leaves, there was an interaction between species and seasons for ABA and PA contents. L. divaricata had high ABA content during spring and low ABA content during autumn; while L. chilense showed the opposite pattern. During spring, drought tolerant species had high PA content while drought avoidant species had low PA content, and during autumn these species showed the opposite pattern. ABA-GE content was highest in L. chilense green leaves. In fine roots, ABA content was highest in L. divaricata and during spring PA was higher in L. divaricata than P. ligularis and L. chilense. PA was the only metabolite that decreased in L. divaricata during autumn. Results showed that ABA homeostasis maintains the functioning of different life forms with different drought resistance strategies in Patagonia semiarid shrublands. In green leaves of the drought avoidant L. chilense shrub, the ABA conjugation pathway was active in both seasons. During spring, the most drought tolerant L. divaricata showed highest activation of ABA synthesis and ABA oxidation pathways. During autumn L. chilense showed highest activation of ABA synthesis and together with P. ligularis showed active the ABA oxidation pathway.

Additional keywords: abscisic acid homeostasis, Larrea divaricata, liquid chromatography-mass spectrometry, Lycium chilense, Pappostipa speciosa, phaseic acid, Poa ligularis.


References

Bertiller MB, Beeskow AM, Coronato FR (1991) Seasonal environmental variation and plant phenology in arid Patagonia (Argentina). Journal of Arid Environments 21, 1–11.
Seasonal environmental variation and plant phenology in arid Patagonia (Argentina).Crossref | GoogleScholarGoogle Scholar |

Boursiac Y, Léran S, Corratgé-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends in Plant Science 18, 325–333.
ABA transport and transporters.Crossref | GoogleScholarGoogle Scholar |

Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Arce ME (2009) Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species. Oecologia 160, 631–641.
Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species.Crossref | GoogleScholarGoogle Scholar |

Bucci S, Scholz FG, Peschiutta ML, Arias NS, Meinzer FC, Goldstein G (2013) The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought-induced embolism by leaves and roots. Plant, Cell & Environment 36, 2163–2174.
The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought-induced embolism by leaves and roots.Crossref | GoogleScholarGoogle Scholar |

Campanella MV, Bertiller MB (2008) Plant phenology, leaf traits and leaf litterfall of contrasting life forms in the arid Patagonian Monte, Argentina. Journal of Vegetation Science 19, 75–85.
Plant phenology, leaf traits and leaf litterfall of contrasting life forms in the arid Patagonian Monte, Argentina.Crossref | GoogleScholarGoogle Scholar |

Campanella MV, Bertiller MB (2009) Leafing patterns and leaf traits of four evergreen shrubs in the Patagonian Monte, Argentina. Acta Oecologica 35, 831–837.
Leafing patterns and leaf traits of four evergreen shrubs in the Patagonian Monte, Argentina.Crossref | GoogleScholarGoogle Scholar |

Carrera AL, Sain CL, Bertiller MB (2000) Patterns of nitrogen conservation in shrubs and grasses in the Patagonian Monte, Argentina. Plant and Soil 224, 185–193.
Patterns of nitrogen conservation in shrubs and grasses in the Patagonian Monte, Argentina.Crossref | GoogleScholarGoogle Scholar |

Cenzano AM, Masciarelli O, Luna MV (2014) Abscisic acid metabolite profiling as indicators of plastic responses to drought in grasses from arid Patagonian Monte (Argentina). Plant Physiology and Biochemistry 83, 200–206.
Abscisic acid metabolite profiling as indicators of plastic responses to drought in grasses from arid Patagonian Monte (Argentina).Crossref | GoogleScholarGoogle Scholar |

Cenzano AM, Varela MC, Luna MV (2016) Ecophysiology of native species from Patagonian Monte, Argentina. In ‘Sabkha ecosystems. Vol. V, The Americas (tasks for vegetation science)’. (Eds MA Khan, B Böer, M Clüsener-Godt, M Öztürk, B Gul) pp. 369–387. (Springer International Publishing AG: Cham, Switzerland)

Chartier MP, Rostagno CM (2006) Soil erosion thresholds and alternative states in northeastern Patagonian rangelands. Rangeland Ecology and Management 59, 616–624.
Soil erosion thresholds and alternative states in northeastern Patagonian rangelands.Crossref | GoogleScholarGoogle Scholar |

Coronato FR, Bertiller MB (1997) Climatic controls of soil moisture dynamics in an arid steppe of Northern Patagonia, Argentina. Arid Soil Research and Rehabilitation 11, 277–288.
Climatic controls of soil moisture dynamics in an arid steppe of Northern Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Coupel-Ledru A, Tyerman SD, Masclef D, Lebon E, Christophe A, Edwards EJ, Simonneau T (2017) Abscisic acid down-regulates hydraulic conductance of grapevine leaves in isohydric genotypes only. Plant Physiology 175, 1121–1134.
Abscisic acid down-regulates hydraulic conductance of grapevine leaves in isohydric genotypes only.Crossref | GoogleScholarGoogle Scholar |

Craine JM (2009) Resource strategies of wild plants. In ‘The basis for plant strategies’. (Ed. JM Craine) pp. 1–14. (Princeton University Press: Princeton, NJ, USA)

Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651–679.
Abscisic acid: emergence of a core signaling network.Crossref | GoogleScholarGoogle Scholar |

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29, 185–212.
Plant drought stress: effects, mechanisms and management.Crossref | GoogleScholarGoogle Scholar |

Fernández OA, Busso CA (1999) Arid and semi-arid rangelands: two thirds of Argentina. Rala Report 200, 41–60.

Givnish TJ (2002) Adaptive significance of evergreen vs deciduous leaves: solving the triple paradox. Silva Fennica 36, 703–743.
Adaptive significance of evergreen vs deciduous leaves: solving the triple paradox.Crossref | GoogleScholarGoogle Scholar |

Golluscio RA, Sala OE, Lauenroth WK (1998) Differential use of large summer rainfall events by shrubs and grasses: a manipulative experiment in the Patagonian steppe. Oecologia 115, 17–25.
Differential use of large summer rainfall events by shrubs and grasses: a manipulative experiment in the Patagonian steppe.Crossref | GoogleScholarGoogle Scholar |

Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JH, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, Hillier SH, Hodkinson DJ, Jalili A, Liu Z, Mackey JML, Matthews N, Mowforth MA, Neal AM, Reader RJ, Reiling K, Ross-Fraser W, Spencer RE, Sutton F, Tasker DE, Thorpe PC, Whitehouse J (1997) Integrated screening validates primary axes of specialization in plants. Oikos 79, 259–281.
Integrated screening validates primary axes of specialization in plants.Crossref | GoogleScholarGoogle Scholar |

Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
The role of stomata in sensing and driving environmental change.Crossref | GoogleScholarGoogle Scholar |

Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proceedings of the National Academy of Sciences of the United States of America 94, 7362–7366.
A global budget for fine root biomass, surface area, and nutrient contents.Crossref | GoogleScholarGoogle Scholar |

Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109–1120.
Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid.Crossref | GoogleScholarGoogle Scholar |

León RJC, Bran D, Collantes M, Paruelo JM, Soriano A (1998) Grandes unidades de vegetación de la Patagonia extra andina. Ecología Austral 8, 125–144.

Loik ME (2007) Sensitivity of water relations and photosynthesis to summer precipitation pulses for Artemisia tridentata and Purshia tridentate. Plant Ecology 191, 95–108.
Sensitivity of water relations and photosynthesis to summer precipitation pulses for Artemisia tridentata and Purshia tridentate.Crossref | GoogleScholarGoogle Scholar |

McLaren JR, Wilson SD, Peltzer DA (2004) Plant feedbacks increase the temporal heterogeneity of soil moisture. Oikos 107, 199–205.
Plant feedbacks increase the temporal heterogeneity of soil moisture.Crossref | GoogleScholarGoogle Scholar |

Moreno L, Bertiller MB (2015) Phenotypic plasticity of morpho-chemical traits of perennial grasses from contrasting environments of arid Patagonia. Journal of Arid Environments 116, 96–102.
Phenotypic plasticity of morpho-chemical traits of perennial grasses from contrasting environments of arid Patagonia.Crossref | GoogleScholarGoogle Scholar |

Noy-Meir I (1973) Desert ecosystems: environment and producers. Annual Review of Ecology and Systematics 4, 25–52.
Desert ecosystems: environment and producers.Crossref | GoogleScholarGoogle Scholar |

Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 8ʹ-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiology 149, 825–834.
High humidity induces abscisic acid 8ʹ-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Pantin F, Simonneau T, Muller B (2012) Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny. New Phytologist 196, 349–366.
Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny.Crossref | GoogleScholarGoogle Scholar |

Paruelo JM, Beltrán A, Jobbágy E, Sala OE, Golluscio RA (1998) The climate of Patagonia: general patterns and control son biotic processes. Ecología Austral 8, 85–101.

Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Garnier E (1999) Ecological significance of inherent variation in relative growth rate and its components. In ‘Handbook of functional plant ecology’. (Eds FI Pugnaire, F Valladares) pp. 81–120. (Marcel Dekker: New York)

Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Australian Journal of Plant Physiology 27, 595–607.
The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review.Crossref | GoogleScholarGoogle Scholar |

Reid JB, Renquist AR (1997) Enhanced root production as a feed-forward response to soil water deficit in field-grown tomatoes. Australian Journal of Plant Physiology 24, 685–692.
Enhanced root production as a feed-forward response to soil water deficit in field-grown tomatoes.Crossref | GoogleScholarGoogle Scholar |

Saura-Mas S, Lloret F (2007) Leaf and shoot water content and leaf dry matter content of Mediterranean woody species with different post-fire regenerative strategies. Annals of Botany 99, 545–554.
Leaf and shoot water content and leaf dry matter content of Mediterranean woody species with different post-fire regenerative strategies.Crossref | GoogleScholarGoogle Scholar |

Sauter A, Dietz KJ, Hartung W (2002) A possible stress physiological role of abscisic acid conjugates in root to shoot signaling. Plant, Cell & Environment 25, 223–228.
A possible stress physiological role of abscisic acid conjugates in root to shoot signaling.Crossref | GoogleScholarGoogle Scholar |

Scholz FG, Bucci SJ, Arias N, Meinzer FC, Goldstein G (2012) Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: coping with drought and subzero temperatures. Oecologia 170, 885–897.
Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: coping with drought and subzero temperatures.Crossref | GoogleScholarGoogle Scholar |

Seiler C, Harshavardhan VT, Rajesh K, Reddy PS, Strickert M, Rolletschek H, Scholz U, Wobus U, Sreenivasulu N (2011) ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. Journal of Experimental Botany 62, 2615–2632.
ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions.Crossref | GoogleScholarGoogle Scholar |

Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. Journal of Experimental Botany 53, 33–37.
ABA, ethylene and the control of shoot and root growth under water stress.Crossref | GoogleScholarGoogle Scholar |

Sharp RE, Wu Y, Voetberg GS, Saab IN, LeNoble ME (1994) Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials. Journal of Experimental Botany 45, 1743–1751.
Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials.Crossref | GoogleScholarGoogle Scholar |

Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. Journal of Experimental Botany 55, 2343–2351.
Root growth maintenance during water deficits: physiology to functional genomics.Crossref | GoogleScholarGoogle Scholar |

Shipley B, Vu TT (2002) Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytologist 153, 359–364.
Dry matter content as a measure of dry matter concentration in plants and their parts.Crossref | GoogleScholarGoogle Scholar |

Spollen W, LeNoble M, Samuels T, Bernstein N, Sharp R (2000) Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiology 122, 967–976.
Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production.Crossref | GoogleScholarGoogle Scholar |

Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506, 265–273.
Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress?Crossref | GoogleScholarGoogle Scholar |

Srivastava LM (2002) Abscisic acid and stress tolerance in plants. In ‘Plant growth and development, Hormones and environment’. (Ed. LM Srivastava) pp. 381–412. (Academic Press: New York)

Tardieu F, Parent B, Simonneau T (2010) Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? Plant, Cell & Environment 33, 636–647.
Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes?Crossref | GoogleScholarGoogle Scholar |

Thomas CK, Law BE, Irvine J, Martin JG, Pettijohn JC, Davis KJ (2009) Seasonal hydrology explains interannual and seasonal variation in carbon and water exchange in a semiarid mature ponderosa pine forest in central Oregon. Journal of Geophysical Research 114, G04006
Seasonal hydrology explains interannual and seasonal variation in carbon and water exchange in a semiarid mature ponderosa pine forest in central Oregon.Crossref | GoogleScholarGoogle Scholar |

Varela MC, Arslan I, Reginato M, Cenzano AM, Luna MV (2016) Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrublands (Argentina). Plant Physiology and Biochemistry 104, 81–91.
Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrublands (Argentina).Crossref | GoogleScholarGoogle Scholar |

Varela MC, Reinoso H, Luna MV, Cenzano AM (2018) Seasonal changes in morphological and hormonal traits of two native Patagonian shrubs from Argentina with different drought resistance strategies. Plant Physiology and Biochemistry 127, 506–515.
Seasonal changes in morphological and hormonal traits of two native Patagonian shrubs from Argentina with different drought resistance strategies.Crossref | GoogleScholarGoogle Scholar |

Westoby M, Falster D, Moles A, Vesk P, Wright I (2002) Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33, 125–159.
Plant ecological strategies: some leading dimensions of variation between species.Crossref | GoogleScholarGoogle Scholar |

Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. Journal of Experimental Botany 59, 3317–3325.
Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass.Crossref | GoogleScholarGoogle Scholar |

Xu ZJ, Nakajima M, Suzuki Y, Yamaguchi I (2002) Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings. Plant Physiology 129, 1285–1295.
Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings.Crossref | GoogleScholarGoogle Scholar |

Yamashita Y, Ota M, Inoue Y, Hasebe Y, Okamoto M, Inukai T, Masuta C, Sakihama Y, Hashidoko Y, Kojima M, Sakakibara H, Inage Y, Takahashi K, Yoshihara T, Matsuura H (2016) Chemical promotion of endogenous amounts of ABA in Arabidopsis thaliana by a natural product, theobroxide. Plant & Cell Physiology 57, 986–999.
Chemical promotion of endogenous amounts of ABA in Arabidopsis thaliana by a natural product, theobroxide.Crossref | GoogleScholarGoogle Scholar |