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Aluminum-induced stress differently modifies Urochloa genotypes responses on growth and regrowth: root-to-shoot Al-translocation and oxidative stress

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Abstract

Forage grasses belonging to the Urochloa (Brachiaria) genus present tolerance to Al toxicity, however there are intra- and interspecific differences among the species, which in turn should be better depicted. Here we evaluate genotypic differences in Al tolerance in four Urochloa (U. decumbens cultivar Basilisk; U. brizantha cultivar Marandu; U. brizantha cultivar Piatã and U. brizantha cultivar Xaraés) cultivated in nutrient solution, during growth and regrowth. We analyzed the effect of Al uptake on epidermal and cell membrane damage, and lipid peroxidation in shoots and roots. Exposure of genotypes to Al concentration up to 1.33 mmol L−1 led to different degrees of shoot yield, mainly during the growth period. Increased Al concentration decreased dry matter production in shoots and roots, reduced leaf area (LA), relative root growth, increased Al accumulation in the roots and root-to-shoot Al translocation, notably during the first growth period. However, Al translocation from roots to shoots augmented massively in all genotypes, during the regrowth. Plant roots exposed to Al were damaged, exhibiting ruptures in the epidermis and reduced number of root hairs. Lipid peroxidation in shoots ranged in all genotypes exposed to Al, however, the oxidative stress was 2–5 times higher in shoots than in roots, notably in Marandu that accumulated 95% more Al than U. decumbens. This suggests that in the genotypes that are more tolerant to Al there is maintenance of metabolic activities, including upregulated and efficient antioxidant activity, root growth, LA growth and biomass yield.

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Abbreviations

DM:

Dry matter

H2O2 :

Hydrogen peroxide

LA:

Leaf area

MDA:

Malondialdehyde

PVPP:

Polyvinylpyrrolidone

RRG:

Relative root growth

SEM:

Scanning electron microscope

TBA:

2-Thiobarbituric acid

TCA:

Trichloroanisole

TRL:

Total root length

References

  • Alcântara BK, Machemer-Noonan K, Silva Junior FG, Azevedo RA (2015) Dry priming of maize seeds reduces aluminum stress. PLoS ONE 12:e0145742. https://doi.org/10.1371/journal.pone.0145742

    Article  CAS  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Arroyave C, Barceló J, Poschenrieder C, Tolrà R (2011) Aluminium-induced changes in root epidermal cell patterning, a distinctive feature of hyperresistance to Al in Urochloa decumbens. J Inorg Biochem 105:1477–1483

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Arroyave C, Tolrà R, Chaves L, de Souza MC, Barceló J, Poschenrieder C (2018) A proteomic approach to the mechanisms underlying activation of aluminum resistance in roots of Urochloa decumbens. J Inorg Biochem 181:145–151

    Article  PubMed  CAS  Google Scholar 

  • Brunner I, Sperisen C (2013) Aluminum exclusion and aluminum tolerance in woody plants. Front Plant Sci 4:172. https://doi.org/10.3389/fpls.2013.00172

    Article  PubMed  PubMed Central  Google Scholar 

  • Capaldi FR, Gratão PL, Reis AR, Lima LW, Azevedo RA (2015) Sulfur metabolism and stress defense responses in plants. Trop Plant Biol 8:60–73

    Article  CAS  Google Scholar 

  • Clark RB (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Desikan R, Cheung MK, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock J, Neill S (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Funct Plant Biol 31:913–920

    Article  CAS  Google Scholar 

  • Giannakoula A, Moustakasa M, Mylonab P, Papadakisc I, Yupsanisd T (2008) Aluminum tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline, and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396

    Article  PubMed  CAS  Google Scholar 

  • Gratão PL, Pole A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    Article  CAS  Google Scholar 

  • Gratão PL, Monteiro CC, Tiago T, Carvalho RF, Alves LR, Peters LP, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. Biometals 28:803–816

    Article  PubMed  CAS  Google Scholar 

  • Guo T, Zhang G, Zhou M, Wu F, Chen J (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248

    Article  CAS  Google Scholar 

  • Guo TR, Zhang GP, Zhang YH (2007) Physiological changes in Barley plants under combined toxicity of aluminum, copper and cadmium. Colloid Surface B 57:182–188

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminum resistance of plants: a review. Ann Bot 106:185–197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kopittke PM, McKenna BA, Karunakaran C, Dynes JJ, Arthur Z, Gianoncelli A, Kourousias G, Menzies NW, Ryan PR, Wang P, Green K, Blamey FPC (2017) Aluminum complexation with malate within the root apoplast differs between aluminum resistant and sensitive wheat lines. Front Plant Sci 8:1377. https://doi.org/10.3389/fpls.2017.01377

    Article  PubMed  PubMed Central  Google Scholar 

  • Lavres Junior J, Ferragine MDC, Gerdes L, Raposo RWC, Costa MNX, Monteiro FA (2004) Yield components and morphogenesis of Aruana grass in response to nitrogen supply. Sci Agric 61:632–639

    Article  Google Scholar 

  • Lavres Junior J, Malavolta E, Nogueira NL, Moraes MF, Reis AR, Rossi ML, Cabral CP (2009) Changes in anatomy and root cell ultrastructure of soybean genotypes under manganese stress. Rev Bras Cienc Solo 33:395–403

    Article  Google Scholar 

  • Lavres Junior J, Reis AR, Rossi ML, Cabral CP, Nogueira NDL, Malavolta E (2010) Changes in the ultrastructure of soybean cultivars in response to manganese supply in solution culture. Sci Agric 67:287–294

    Article  Google Scholar 

  • Lee YP, Kim SH, Bang JW, Lee HS, Kwak SS, Kwon SY (2007) Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. Plant Cell Rep 26:591–598

    Article  PubMed  CAS  Google Scholar 

  • Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867. https://doi.org/10.3389/fpls.2017.01867

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    Article  PubMed  CAS  Google Scholar 

  • Nogueirol RC, Monteiro FA, Gratão PL, Borgo L, Azevedo RA (2015) Tropical soils with high aluminum concentrations cause oxidative stress in two tomato genotypes. Environ Monit Assess 187:73–89

    Article  PubMed  CAS  Google Scholar 

  • Poozesh V, Cruz P, Choler P, Bertoni G (2007) Relationship between the Al resistance of grasses and their adaptation to an infertile habitat. Ann Bot 99:947–954

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rabêlo FHS, Fernie AR, Navazas A, Borgo L, Keunen E, Silva BKA, Cuypers A, Lavres J (2018) A glimpse into the effect of sulfur supply on metabolite profiling, glutathione and phytochelatins in Panicum maximum cv. Massai exposed to cadmium. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2018.04.003

    Article  Google Scholar 

  • Ramos FT, França MGC, Alvim MN, Rossiello ROP, Zonta E (2012) Aluminum tolerance measured by root growth and mucilage protection in Urochloa brizantha and Urochloa decumbens. J Plant Interact 7:225–229

    Article  CAS  Google Scholar 

  • Rangel AF, Rao IM, Horst WJ (2009) Intracellular distribution and binding state of aluminum in root apices of two commom bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiol Plantarum 135:162–173

    Article  CAS  Google Scholar 

  • Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang WH, Delhaize E (2011) The identification of aluminum-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62:9–20

    Article  PubMed  CAS  Google Scholar 

  • Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214

    Article  CAS  Google Scholar 

  • Tamás L, Huttová J, Mistrík I (2003) Inhibiton of Al-induced root elongation and enhancement of Al-induced peroxidase activity in Al-sensitive and Al-resistant barley cultivars are positively correlated. Plant Soil 250:193–200

    Article  Google Scholar 

  • Vitoria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    Article  PubMed  CAS  Google Scholar 

  • Von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • Wang Y, Stass A, Horst WJ (2004) Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol 136:3762–3770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watanabe T, Osaki M, Yano H, Rao I (2006) Internal mechanisms of plant Adaptation to aluminum toxicity and phosphorus starvation in three tropical forages. J Plant Nutr 29:1243–1255

    Article  CAS  Google Scholar 

  • Wenzl P, Patiño GM, Chaves AL, Mayer JE, Rao IM (2001) The high level of aluminum resistance in signalgrass is not associated with known mechanisms of external aluminum detoxification in root apices. Plant Physiol 125:1473–1484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wenzl P, Chaves AL, Patiño GM, Mayer JE, Rao IM (2002) Aluminum stress stimulates the accumulation of organic acids in root apices of Urochloa species. J Plant Nutr Soil Sc 165:582–588

    Article  CAS  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2003) Oxidative stress triggered by aluminum in plant roots. Plant Soil 255:239–243

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by São Paulo Research Foundation (Fapesp) (grant #2013/02986-0).

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Correspondence to José Lavres.

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Furlan, F., Borgo, L., Rabêlo, F.H.S. et al. Aluminum-induced stress differently modifies Urochloa genotypes responses on growth and regrowth: root-to-shoot Al-translocation and oxidative stress. Theor. Exp. Plant Physiol. 30, 141–152 (2018). https://doi.org/10.1007/s40626-018-0109-2

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