Skip to main content
Log in

Physiological and molecular analysis on root growth associated with the tolerance to aluminum and drought individual and combined in Tibetan wild and cultivated barley

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The drought-stimulated gene expression of NCED, SUS, and KS - DHN and ABA signal cross-talk with other phytohormones maintains barley root growth under drought stress at pH 4.0 plus polyethylene glycol plus aluminum.

Aluminum (Al) toxicity and drought are two major factors that limit barley production. In this work, the individual and combined effects of Al/acid and polyethylene glycol (PEG 6000) induced drought stress that suppressed root growth and caused oxidative damage as characterized by increased H2O2 and \(\text{O}_{2}^{\cdot -}\) accumulation. The wild-barley genotypes, XZ5 and XZ29, exhibited a higher tolerance than the two cultivars Dayton (Al tolerant) and Tadmor (drought tolerant) under combined stress (pH 4.0 + PEG + Al). The oxidative damage induced by PEG was more severe at pH 4.0 than at pH 6.0. In XZ29, the highest root secretion of malate and citrate was recorded, and the least Al uptake in the four genotypes. In XZ5, a peak accumulation of ABA and minor synthesis of zeatin riboside and ethylene were found being essential in maintaining primary root elongation and root hair development. PEG-induced drought stress repressed Al uptake in root tips, with a lower increase in callose formation and HvMATE (Hordeum vulgare multidrug and toxic compound exudation) expression compared to Al-induced callose production. Stress by pH 4.0 + PEG + Al up-regulated 9-cis-epoxycarotenoid dioxygenase (NCED) which is involved in ABA biosynthesis. Such treatment stimulated the regulation of ABA-dependent genes sucrose synthase (SUS) and KS-type dehydrin (KS-DHN) in root tips. Our results suggest that the tolerance ranking to pH 4.0 + PEG + Al stress in Tibetan wild barley by gene expression is closely correlated to physiological indices. The results show that acclimatisation to pH 4.0 + PEG + Al stress involves specific responses in XZ5 and XZ29. The present study provides insights into the effects of Al/acid and drought combined stress on the abundance of physiological indices in the roots of barley varieties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

ACCO:

1-Aminocyclopropane-1-carboxylic acid oxidase

KS-DHN:

KS-type dehydrin

MATE:

Multidrug and toxic compound exudation

\(\text{O}_{2}^{\cdot -}\) :

Super oxide

NCED:

9-cis-epoxycarotenoid dioxygenase

PEG:

Polyethylene glycol

SUS:

Sucrose synthase 2

ZR:

Zeatin riboside

References

  • Ahmed IM, Dai H, Zheng W, Cao F, Zhang GP, Sun D, Wu FB (2013) Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiol Biochem 63:49–60

    Article  CAS  PubMed  Google Scholar 

  • Ahmed IM, Nadira UA, Bibi N, Cao F, He X, Zhang GP, Wu FB (2015) Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environ Exp Bot 111:1–12

    Article  CAS  Google Scholar 

  • Arroyave C, Tolrà R, Thuy T, Barceló J, Poschenrieder C (2013) Differential aluminum resistance in Brachiaria species. Environ Exp Bot 89:11–18

    Article  CAS  Google Scholar 

  • Barceló J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92

    Article  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Beebe S, Ramirez J, Jarvis A, Rao IM, Mosquera G, Bueno JM, Blair MW (2011) Genetic improvement of common beans and the challenges of climate change. In: Yadav SS, Redden RJ, Hatfield JL, Lotze-Campen H, Hall AE (eds) Crop adaptation to climate change. Wiley-Blackwell, Oxford, pp 356–369

    Chapter  Google Scholar 

  • Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR (2004) The Arabidopsis thaliana abscisic acid-insensitive 8 encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16:406–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai S, Wu D, Jabeen Z, Huang Y, Huang Y, Zhang GP (2013) Genome-wide association analysis of aluminum tolerance in cultivated and Tibetan wild barley. PLoS ONE 8:e69776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaves MM, Oliveira M (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384

    Article  CAS  PubMed  Google Scholar 

  • Chen X-Y, Kim J-Y (2004) Callose synthesis in higher plants. Plant Signal Behav 4:489–492

    Article  Google Scholar 

  • Colmenero-Flores JM, Moreno LP, Smith CE, Covarrubias AA (1999) Pvlea-18, a member of a new late-embryogenesis-abundant protein family that accumulates during water stress and in the growing regions of well-irrigated bean seedlings. Plant Physiol 120:93–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Souza TC, Magalhães PC, de Castro EM, Carneiro NP, Padilha FA, Júnior CCG (2014) ABA application to maize hybrids contrasting for drought tolerance: changes in water parameters and in antioxidant enzyme activity. Plant Growth Regul 73:205–217

    Article  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Forster B, Ellis R, Moir J, Talame V, Sanguineti M, Tuberosa R, This D, Teulat-Merah B, Ahmed I, Mariy S (2004) Genotype and phenotype associations with drought tolerance in barley tested in North Africa. Ann Appl Biol 144:157–168

    Article  Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    Article  CAS  PubMed  Google Scholar 

  • Goldman I, Carter T, Patterson R (1989) A detrimental interaction of subsoil aluminum and drought stress on the leaf water status of soybean. Agron J 81:461–463

    Article  CAS  Google Scholar 

  • Hartung W, Sauter A, Hose E (2002) Abscisic acid in the xylem: where does it come from, where does it go to? J Exp Bot 53:27–32

    Article  CAS  PubMed  Google Scholar 

  • Horst WJ, Püschel A-K, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil 192:23–30

    Article  CAS  Google Scholar 

  • Ishikawa H, Evans ML (1993) The role of the distal elongation zone in the response of maize roots to auxin and gravity. Plant Physiol 102:1203–1210

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Köhle H, Jeblick W, Poten F, Blaschek W, Kauss H (1985) Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process. Plant Physiol 77:544–551

    Article  PubMed  PubMed Central  Google Scholar 

  • Kollmeier M, Felle HH, Horst WJ (2013) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956

    Article  Google Scholar 

  • Liu X, Hua X, Guo J, Qi D, Wang L, Liu Z, Jin Z, Chen S, Liu G (2013) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotech Lett 30:1275–1280

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  CAS  PubMed  Google Scholar 

  • Massot N, Poschenrieder C, Barcelo J (1994) Aluminium-induced increase of zeatin riboside and dihydrozeatin riboside in Phaseolus vulgaris L. cultivars. J Plant Nutr 17:255–265

    Article  CAS  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37

    Article  PubMed  PubMed Central  Google Scholar 

  • Nayyar H, Walia D (2003) Water stress induced proline accumulation in contrasting wheat genotypes as affected by calcium and abscisic acid. Biol Plant 46:275–279

    Article  CAS  Google Scholar 

  • Nian H, Yang Z, Huang H, Yan X, Matsumoto H (2005) Combined effect of short-term water deficit stress and aluminum toxicity on citrate secretion from soybean roots. J Plant Nutr 27:1281–1293

    Article  Google Scholar 

  • Nishimura MT, Stein M, Hou B-H, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    Article  CAS  PubMed  Google Scholar 

  • Qin X, Zeevaart JA (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rama Devi S, Prasad M (1998) Copper toxicity in Ceratophyllum demersum L. (Coontail), a free floating macrophyte: response of antioxidant enzymes and antioxidants. Plant Sci 138:157–165

    Article  Google Scholar 

  • Růžička K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446

    Article  CAS  Google Scholar 

  • Saab IN, Sharp RE, Pritchard J (1992) Effect of inhibition of abscisic acid accumulation on the spatial distribution of elongation in the primary root and mesocotyl of maize at low water potentials. Plant Physiol 99:26–33  

  • Saftner RA, Wyse RE (1984) Effect of plant hormones on sucrose uptake by sugar beet root tissue discs. Plant Physiol 74:951–955

  • Serraj R, Sinclair T (2002) Osmolyte accumulation can it really help increase crop yield under drought conditions? Plant, Cell Environ 25:333–341

    Article  Google Scholar 

  • Sharp R (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant, Cell Environ 25:211–222

    Article  CAS  Google 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. J Exp Bot 55:2343–2351

    Article  CAS  PubMed  Google Scholar 

  • Shimazaki Y, Ookawa T, Hirasawa T (2005) The root tip and accelerating region suppress elongation of the decelerating region without any effects on cell turgor in primary roots of maize under water stress. Plant Physiol 139:458–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva S, Pinto-Carnide O, Martins-Lopes P, Matos M, Guedes-Pinto H, Santos C (2010) Differential aluminium changes on nutrient accumulation and root differentiation in an Al sensitive vs. tolerant wheat. Environ Exp Bot 68:91–98

    Article  CAS  Google Scholar 

  • Silva S, Santos C, Matos M, Pinto-Carnide O (2011) Al toxicity mechanisms in tolerant and sensitive rye genotypes. Environ Exp Bot 75:89–97

    Article  Google Scholar 

  • Souter M, Topping J, Pullen M, Friml J, Palme K, Hackett R, Grierson D, Lindsey K (2002) hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14:1017–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staß A, Horst W (2009) Callose in abiotic stress. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1 → 3)-β-glucans and related polysaccharides. Academic Press, New York, pp 499–524

    Chapter  Google Scholar 

  • Wang HL, Lee PD, Chen WL, Huang DJ, Su JC (2000) Osmotic stress-induced changes of sucrose metabolism in cultured sweet potato cells. J Exp Bot 51:1991–1999

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115:265–276

    Article  CAS  PubMed  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu FB, Zhang GP, Dominy P (2003) Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environ Exp Bot 50:67–78

    Article  CAS  Google Scholar 

  • Yamaguchi M, Sharp RE (2010) Complexity and coordination of root growth at low water potentials: recent advances from transcriptomic and proteomic analyses. Plant, Cell Environ 33:590–603

    Article  CAS  Google Scholar 

  • Yang Z-B, Eticha D, Rao IM, Horst WJ (2010) Alteration of cell-wall porosity is involved in osmotic stress-induced enhancement of aluminium resistance in common bean (Phaseolus vulgaris L.). J Exp Bot 61:3245–3258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang ZB, Eticha D, Rotter B, Rao IM, Horst WJ (2011) Physiological and molecular analysis of polyethylene glycol-induced reduction of aluminium accumulation in the root tips of common bean (Phaseolus vulgaris L.). New Phytol 192:99–113

    Article  CAS  PubMed  Google Scholar 

  • Yang Z-B, Eticha D, Albacete A, Rao IM, Roitsch T, Horst WJ (2012) Physiological and molecular analysis of the interaction between aluminium toxicity and drought stress in common bean (Phaseolus vulgaris L.). J Exp Bot 63:3109–3125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang ZB, Rao IM, Horst WJ (2013) Interaction of aluminium and drought stress on root growth and crop yield on acid soils. Plant Soil 372:3–25

    Article  CAS  Google Scholar 

  • Zeng F, Wu X, Qiu B, Wu FB, Jiang L, Zhang GP (2014) Physiological and proteomic alterations in rice (Oryza sativa L.) seedlings under hexavalent chromium stress. Planta 239:91–108

    Article  Google Scholar 

  • Zhao Z, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta 217:794–800

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Sun H, Dai H, Zhang GP, Wu FB (2010) Difference in response to drought stress among Tibet wild barley genotypes. Euphytica 172:395–403

    Article  CAS  Google Scholar 

  • Zheng SJ, Yang JL, He YF, Yu XH, Zhang L, You JF, Shen RF, Matsumoto H (2005) Immobilization of aluminum with phosphorus in roots is associated with high aluminum resistance in buckwheat. Plant Physiol 138:297–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The project was supported by National Natural Science Foundation of China (31171488), National 863 Program (2012AA101105), Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China, and the Key Research Foundation of Science and Technology Department of Zhejiang Province of China (2012C12902-2), and the 56th China Postdoctoral Scientific Research Foundation (517000-X91408). We appreciate Ms Mei Li from the Analysis Center of Agrobiology and Environmental Sciences of Zhejiang University, for her kind help with the experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Feibo Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 221 kb)

425_2015_2442_MOESM2_ESM.tif

Supplemental Fig. S1 Histochemical detection of H2O2 (a) and \(\text{O}_{2}^{\cdot -}\) (b) in barley roots. Barley seedlings were exposed to pH, PEG and Al alone and combined (pH 4.0 + PEG + Al) stresses for 7 days. For details of experimental procedures, see Materials and methods. Scale bar 1 mm (TIFF 2115 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmed, I.M., Nadira, U.A., Cao, F. et al. Physiological and molecular analysis on root growth associated with the tolerance to aluminum and drought individual and combined in Tibetan wild and cultivated barley. Planta 243, 973–985 (2016). https://doi.org/10.1007/s00425-015-2442-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2442-x

Keywords

Navigation