High aluminum concentration and initial establishment of Handroanthus impetiginosus: clues about an Al non-resistant species in Brazilian Cerrado

Abstract

Cerrado soils are acidic and nutrient-poor, with high content of solubilized Al³⁺. Plants growing in these conditions may display adaptations to cope with high aluminum concentrations especially during early developmental stages. We investigated leaf nutritional status, and photosynthetic and growth characteristics during the initial establishment of Handroanthus impetiginosus (Mart. Ex Dc.) Mattos, a secondary tree species distributed in the Brazilian Cerrado. Our goal was to understand leaf-level traits related to different aluminum concentrations. H. impetiginosus plants were cultivated in four different aluminum sulfate concentrations: 0, 1, 2, and 4 mM Al, for 40 days. We performed analyses of growth, leaf gas exchange, chloroplast pigment content, and leaf mineral nutrients. We observed a linear increase of Al leaf content as a function of Al concentration in the nutrient solution. Plants grown in 1 mM Al showed a remarkable increase of K leaf content, net photosynthesis, stomatal conductance, and transpiration, while in 4 mM Al there were reductions of N, P, and K contents, gas exchange characteristics, and height. H. impetiginosus did not have mechanisms of avoidance, compartmentalization, or resistance to high Al concentrations. Indeed, this species showed a hormetic response, with low Al concentrations stimulating and high Al concentrations inhibiting plant responses.

Keywords

Hormesis / Low Al concentration / Al toxicity / Cerrado species / Carbon assimilation

References

[1] Agathokleous E, Kitao M, Calabrese EJ. Hormesis: a compelling platform for sophisticated plant science. Trends Plant Sci, 2019, 24: 318-327.

[2] Agathokleous E, Kitao M, Harayama H, Calabrese EJ. Temperature-induced hormesis in plants. J For Res, 2019, 30: 13-20.

[3] Banhos OFAA, Brenda BM, da Veiga EB Aluminum-induced decrease in CO₂ assimilation in “Rangpur” lime is associated with low stomatal conductance rather than low photochemical performances. Sci Hortic (Amsterdam), 2016, 205: 133-140.

[4] Banhos OFAA, de Souza MC, Habermann G. High aluminum availability may affect Styrax camporum, an Al non-accumulating species from the Brazilian savanna. Theor Exp Plant Physiol, 2016, 28: 321-332.

[5] Bojórquez-Quintal E, Escalante-Magaña C, Echevarría-Machado I, Martínez-Estévez M. Aluminum, a friend or foe of higher plants in acid soils. Front Plant Sci, 2017, 8: 1-18.

[6] Brunner I, Sperisen C. Aluminum exclusion and aluminum tolerance in woody plants. Front Plant Sci, 2013, 4: 1-12.

[7] Calabrese EJ, Blain RB. Hormesis and plant biology. Environ Pollut, 2009, 157: 42-48.

[8] Calabrese EJ, Agathokleous E, Kozumbo WJ Estimating the range of the maximum hormetic stimulatory response. Environ Res, 2019, 170: 337-343.

[9] de Souza MC, Habermann G, do Amaral CL, Rosa AL, Pinheiro MHO, da Costa FB. Vochysia tucanorum Mart.: an aluminum-accumulating species evidencing calcifuge behavior. Plant Soil, 2017, 419: 377-389.

[10] Evans JR. Photosynthesis and nitrogen relationships in leaves of C₃ plants. Oecologia, 1989, 78: 9-19.

[11] Fageria NK. Efeito da calagem na produção de arroz, feijão, milho e soja em solo de cerrado. Pesqui Agropecu Bras, 2001, 36: 1419-1424.

[12] Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, Sato K, Nakazono M, Ma JF. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun, 2012, 3: 713-719.

[13] Guo P, Qi YP, Cai YT, Yang TY, Yang LT, Huang ZR, Chen LS. Aluminum effects on photosynthesis, reactive oxygen species and methylglyoxal detoxification in two Citrus species differing in aluminum tolerance. Tree Physiol, 2018, 38: 1548-1565.

[14] Hajiboland R, Bahrami Rad S, Barceló J, Poschenrieder C. Mechanisms of aluminum-induced growth stimulation in tea (Camellia sinensis). J Plant Nutr Soil Sci, 2013, 176: 616-625.

[15] Haridasan M. Nutritional adaptations of native plants of the cerrado biome in acid soils. Braz J Plant Physiol, 2008, 20: 183-195.

[16] Hoagland DR, Arnon DI. The water culture method for growing plants without soils, 1950, Berkeley: California Agricultural Experimental Station 347

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

[18] Jones HG. Plants and microclimate: a quantitative approach to environmental plant physiology, 1992 2 Cambridge: Cambridge University Press 85

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

[20] Kochian LV, Piñeros MA, Liu J, Magalhaes JV. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol, 2015, 66: 571-598.

[21] Lidon FC, Barreiro MG, Ramalho JC, Lauriano JA. Effects of aluminum toxicity on nutrient accumulation in maize shoots: implications on photosynthesis. J Plant Nutr, 1999, 22: 397-416.

[22] Long A, Zhang J, Yang L-T, Ye X, Lai N-W, Tan L-L, Lin D, Chen L-S. Effects of low pH on photosynthesis, related physiological parameters, and nutrient profiles of Citrus. Front Plant Sci, 2017, 8: 1-22.

[23] Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, 2008 5 Nova Odessa: Instituto Plantarum 384

[24] Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, van Bodegom PM, Cornwell WK, Ellsworth D, Niinemets U, Ordonez A, Reich PB, Santiago LS. Global effects of soil and climate on leaf photosynthetic traits and rates. Glob Ecol Biogeogr, 2015, 24: 706-717.

[25] Malavolta E, Vitti GC, Oliveira SA. Avaliação do estado nutricional das plantas: princípios e aplicações, 1997 2 Piracicaba: Potafos 319

[26] Malta PG, Arcanjo-Silva S, Ribeiro C, Campos NV, Azevedo AA. Rudgea viburnoides (Rubiaceae) overcomes the low soil fertility of the Brazilian Cerrado and hyperaccumulates aluminum in cell walls and chloroplasts. Plant Soil, 2016, 408: 369-384.

[27] Matsumoto H. Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Citol, 2000, 200: 1-46.

[28] Miatto RC, Wright IJ, Batalha MA. Relationships between soil nutrient status and nutrient-related leaf traits in Brazilian cerrado and seasonal forest communities. Plant Soil, 2016, 404: 13-33.

[29] Mihailovic N, Drazic G, Vucinic Z. Effects of aluminium on photosynthetic performance in Al-sensitive and Al-tolerant maize inbred lines. Photosynthetica, 2008, 46: 476-480.

[30] Monteiro VFC 2014 Crescimento radial e resposta ecofisiológica de Vochysia thyrsoidea (Pohl.) às condições ambientais do cerrado rupestre. Dissertation, Universidade Federal de Lavras, Lavras, p 84

[31] Moreno-Alvarado M, García-Morales S, Trejo-Téllez LI, Hidalgo-Contreras JV, Gómez-Merino FC. Aluminum enhances growth and sugar concentration, alters macronutrient status and regulates the expression of NAC transcription factors in rice. Front Plant Sci, 2017, 8: 1-16.

[32] Muhammad N, Zvobgo G, Guo-ping Z. A review: the beneficial effect of aluminum on plant growth in acid soil and the possible mechanisms. J Integr Agric, 2018, 17: 60345-60347.

[33] Pandey R, Zinta G, AbdElgawad H, Ahmad A, Jain V, Janssens IA. Physiological and molecular alterations in plants exposed to high [CO₂] under phosphorus stress. Biotechnol Adv, 2015, 33: 303-316.

[34] Ribeiro MAQ, de Almeida AAF, Mielke MS, Gomes FP, Pires MV, Baligar VC. Aluminum effects on growth, photosynthesis, and mineral nutrition of cacao genotypes. J Plant Nutr, 2013, 36: 1161-1179.

[35] Ridolfi M, Garrec J-P. Consequences of an excess Al and a deficiency in Ca and Mg for stomatal functioning and net carbon assimilation of beech leaves. Ann For Sci, 2000, 57: 209-218.

[36] Rossatto DR, Carvalho FA, Haridasan M. Soil and leaf nutrient content of tree species support deciduous forests on limestone outcrops as a eutrophic ecosystem. Acta Bot Bras, 2015, 29: 231-238.

[37] Sade H, Meriga B, Surapu V, Gadi J, Sunita MSL, Suravajhala P, Kishor PBK. Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils. Biometals, 2016, 29: 187-210.

[38] Salomão AN, Camilo J. Vieira RF, Camillo J, Coradin L. Handroanthus impetiginosus. Espécies nativas da flora brasileira de valor econômico atual ou potencial, 2016, Brasília: Ministério do Meio Ambiente 801 812

[39] Scolforo JRS. Faleiro FG, Farias Neto AL. Características e produção das fisionomias do Cerrado em Minas Gerais. Savanas: desafios e estratégias para o equilíbrio entre sociedade, agronegócio e recursos naturais, 2008, Planaltina: Embrapa Cerrado 505 610

[40] Siqueira Neto M, De Cássia Piccolo M, Scopel E, Da Costa Júnior C, Cerri CC, Bernoux EM. Carbono total e atributos químicos com diferentes usos do solo no cerrado. Acta Sci Agron, 2009, 31: 709-717.

[41] Team RDC, R Development Core Team R (2016) R: a language and environment for statistical computing. R Found Stat Comput.

[42] Wang C, Wood FA. A modified aluminon reagent for the determination of aluminum after HNO₃-H₂SO₄ digestion. Can J Soil Sci, 1973, 53: 237-239.

[43] Wang L, Fan XW, Pan JL, Huang ZB, Li YZ. Physiological characterization of maize tolerance to low dose of aluminum, highlighted by promoted leaf growth. Planta, 2015, 242: 1391-1403.

[44] Yang M, Tan L, Xu Y, Zhao Y, Cheng F, Ye S, Jiang W. Effect of low pH and aluminum toxicity on the photosynthetic characteristics of different fast-growing Eucalyptus vegetatively propagated clones. PLoS ONE, 2015, 10: 1-15.