Ecophysiological response of Astronium fraxinifolium (Anacardiaceae) in degraded and non-degraded brazilian Cerrado

Marilaine Cristina Marques Leite Maycon Anderson Araujo Lucas Anjos Souza Aline Redondo Martins Liliane Santos Camargos About the authors

Abstract

Plants native from Cerrado generally have peculiar characteristics that allow tolerating water and nutritional stress. Astronium fraxinifolium is a Anacardiaceae tree of from Brazilian Cerrado. The aim of this research was to characterize A. fraxinifolium leaves morphophysiologically, in order to recognize characteristics related to acclimatization of the species in different soil conditions. Two populations of A. fraxinifolium were sampled in different study areas, A1 (Degraded Soil) and A2 (“Undegraded Soil”). Nitrogen compounds, total carbohydrates, chlorophyll, nutritional content, stomatal density and gas exchanges were quantified, comparing the areas. A high number of stomata was observed on the abaxial surface of A. fraxinifolium leaves, with a higher density occurring in A1 individuals. The values ​​of chlorophyll and boron content were significantly higher in A2 plants. It’s possible that the lowest concentration of boron in A1 plants is related to chlorophyll production. Regardinf the other analysis, there weren’t significant differences between the areas. The results show that this species undergoes changes in production of chlorophyll, but liquid photosynthesis isn’t impaired, considering the low chlorophyll content in A1 being compensated by the higher stomatal density. Thus, these changes may be the result of acclimating this species to different environmental conditions to which it’s exposed.

Key words
chlorophyll content; nutritional deficiency; physiological characterization; stomatal density

Resumo

Plantas nativas do Cerrado geralmente apresentam características peculiares que permitem tolerar o estresse hídrico e nutricional. Astronium fraxinifolium, é uma das espécies arbóreas de Anacardiaceae do Cerrado brasileiro. O objetivo desta pesquisa foi caracterizar morfofisiologicamente as folhas de A. fraxinifolium, com o objetivo de reconhecer características relacionadas a aclimatação da espécie em diferentes condições de solo. Para tanto, duas populações de A. fraxinifolium foram amostradas em diferentes áreas de estudo, A1 (Solo degradado) e A2 (“Solo não degradado”). A partir dessas amostras foram quantificados compostos nitrogenados, carboidratos totais, amido, clorofila, conteúdo nutricional, densidade estomática, trocas gasosas, alocação de carbono e altura da parte aérea, comparando as áreas de estudo. Um número elevado de estômatos foi observado na superfície abaxial das folhas de A. fraxinifolium, com uma densidade estomática mais elevada ocorrendo em indivíduos de A1. Já os valores de clorofila a, b e total foram significativamente maiores em A2. O conteúdo nutricional não diferiu entre as áreas, exceto o boro, que apresenta maior concentração nas plantas de A2. É possível que a menor concentração de boro nas plantas A1 esteja relacionado a produção de clorofila. Em relação às demais análises, não houve diferenças significativas entre as áreas. Os resultados mostram que esta espécie sofre alterações na produção de clorofila, mas a fotossíntese líquida não é perturbada, sendo o baixo teor de clorofila em A1 compensado pela maior densidade estomática. Assim, essas mudanças podem ser o resultado da aclimatação dessa espécie às diferentes condições ambientais às quais está exposta.

Palavras-chave
teor de clorofila; deficiência nutricional; caracterização fisiológica; densidade estomática

Introduction

Due to human activities, there has been a progressive increase in the environmental degradation events (De Long et al. 2015De Long C, Cruse R & Wiener J (2015) The soil degradation paradox: compromising our resources when we need them the most. Sustainability 7: 866-879.). Soil degradation directly affects local vegetation once soil conditions is one of the determinant factors to the development of plants, and so it may directly compromise the infiltration capacity (Deon et al. 2018Deon RC, Zilli D, Brandelero G & Machado RG (2018) Compaction and water infiltration capacity of a cambisol by the traffic of machines and cattle trampling Ciência Agrícola 16: 77-84.), soil water storage and root growth (Dinis et al. 2015Dinis C, Surový P, Ribeiro N & Oliveira MRG (2015) The effect of soil compaction at different depths on cork oak seedling growth. New Forests 46: 235-246.; Cambi et al. 2017Cambi M, Mariotti B, Fabiano F, Maltoni A, Tani A, Foderi C, Laschi A & Marchi E (2017) Early response of Quercus robur seedlings to soil compaction following germination. Land Degradation & Development 29: 916-925.).

Thus, environmental factor such as soil conditions, water, light, temperature, etc., influence the morphophysiological characteristics of the plants and so, environmental changes can cause structural changes (Costa et al. 2012Costa VP, Hayashi AH, Carvalho MAM & Silva EA (2012) Aspectos fisiológicos, anatômicos e ultra-estruturais do rizoma de Costus arabicus L. (Costaceae) sob condições de déficit hídrico. Hoehnea 39: 125-137.; Alameda & Villar 2012Alameda D & Villar R (2012) Linking root traits to plant physiology and growth in Fraxinus angustifolia Vahl. seedlings under soil compaction conditions. Environmental Experimental Botany 79: 49-57.; Aref et al. 2013Aref IM, Ahmed AI, Khan PR, El-Atta HA & Iqbal M (2013) Drought-induced adaptive changes in the seedling anatomy of Acacia ehrenbergiana and Acacia tortilis subsp. raddiana. Trees 27: 959- 971.; Cambi et al. 2016Cambi M, Hoshika Y, Mariotti B, Paoletti E, Picchio R, Venanzi R & Marchi E (2016) Compaction by a forest machine affects soil quality and Quercus robur L. seedling performance in an experimental field. Forest Ecology and Management 384: 406-414.) and physiological (Warren et al. 2011Warren CR, Aranda I & Cano FJ (2011) Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant, Cell & Environment 34: 1609-1629.; Alameda & Villar 2012Alameda D & Villar R (2012) Linking root traits to plant physiology and growth in Fraxinus angustifolia Vahl. seedlings under soil compaction conditions. Environmental Experimental Botany 79: 49-57.; Lu et al. 2012Lu P, Chacko EK, Bithell SL, Schaper H, Wiebel J, Cole S & Muller WJ (2012) Photosynthesis and stomatal conductance of five mango cultivars in the seasonally wet-dry tropics of northern Australia. Scientia Horticulturae 138: 108-119.; Cambi et al. 2016Cambi M, Hoshika Y, Mariotti B, Paoletti E, Picchio R, Venanzi R & Marchi E (2016) Compaction by a forest machine affects soil quality and Quercus robur L. seedling performance in an experimental field. Forest Ecology and Management 384: 406-414.; Wang et al. 2018Wang L, Chang J, Zheng X, Liu J, Yu M, Liu L, Yang Y & Zhang H (2018) Survey of ecological environmental conditions and influential factors for public parks in Shanghai. Chemosphere 190: 9-16.).

In the literature there are several reports of natural regeneration in sites with degraded soils with growth of several species representing several taxa (Ferreira et al. 2010Ferreira WC, Botellho AS, Davide AC, Faria JMR & Ferreira DF (2010) Regeneração natural como indicador de recuperação de área degradada a jusante da usina hidrelétrica de Camargos, MG. Revista Árvore 34: 651-660.; Araújo et al. 2006Araújo FS, Martins SV, Meira Neto JAA, Lani JL & Pires IE (2006) Estrutura da vegetação arbustivo-arbórea colonizadora de uma área degradada por mineração de caulim, Brás Pires, MG. Revista Árvore 30: 107-116.; Higuchi et al. 2006Higuchi P, Reis MGF, Reis GG, Pinheiro AL, Silva CT & Oliveira CHR (2006) Composição florística da regeneração natural de espécies arbóreas ao longo de oito anos em um fragmento de floresta estacional semidecidual, em Viçosa, MG. Revista Árvore 30: 893-904.; Gama et al. 2002Gama JRV, Botelho AS & Bentes-Gama MM (2002) Composição florística e estrutura da regeneração natural de floresta secundária de várzea baixa no estuário amazônico. Revista Árvore 26: 559-566.; Campos & Landgraf 2001Campos JC & Landgraf PRC (2001) Análise da regeneração natural de espécies florestais em matas ciliares de acordo com a distância da margem do lago. Ciência Florestal 11: 143-151.). These observations indicate the high capacity of these plants to acclimatise to environmental changes. For example, xerophytic species exhibit adaptive characteristics that allow them to survive in rocky soils with low nutrient availability and undergoing large periods of drought (Fahn & Cutler 1992Fahn A & Cutler D (1992) Handbuch der pflanzen anatomie encyclopedia of plant anatomy Traité d’ Anatomie Végétale: Xerophytes. Vol. 1. Ed. Gebrüder Borntraeger, Berlin. 176p.).

A species that occurs in high frequency in recovering degraded areas in the Brazilian Cerrado is Astronium fraxinifolium Schott (Venturoli et al. 2011Venturoli F, Felfili JM & Fagg CW (2011) Avaliação temporal da regeneração natural em uma floresta estacional semidecídua secundária, em Pirenópolis, Goiás. Revista Árvore 35: 473-483.; Marangon et al. 2008Marangon LC, Soares JJ, Feliciano ALP & Silva e Brandão CFL (2008) Regeneração natural em um fragmento de floresta estacional semidecidual em Viçosa, Minas Gerais. Revista Árvore 32: 183-191.; Neri et al. 2005Neri AV, Campos EP, Duarte TG, Meira Neto JAA, Silva AF & Valente GE (2005) Regeneração de espécies nativas lenhosas sob plantio de Eucalyptus em área de Cerrado na Floresta Nacional de Paraopeba, MG, Brasil. Acta Botanica Brasilica 19: 369-376.). It is commonly known as “Gonçalo-Alves”, and it is a pioneer, deciduous, heliophyte, native xerophytic tree plant from the Cerrado (Lorenzi 2002Lorenzi H (2002) Árvores Brasileiras. 4th ed. Ed. Instituto Plantarum, Nova Odessa. 368p.).

Considering that environmental changes, such as degradation, can cause modifications in plant morphophysiology the present study aimed to evaluates morphology and physiology of the leaves of Astronium fraxinifolium, in order to verify the occurrence of morphophysiological changes in two populations species occurring in non-degraded and degraded areas and too evaluate the soil physical-quality by the construction of the dam of the Ilha Solteira hydroelectric power plant, Brazil. Therefore, we evaluated the stomatal density, specific leaf area, gas exchange, nutritional status, chlorophyll content, quantification of nitrogen compounds, total carbohydrate and starch.

Material and Methods

The botanical material was sampled at FEPE (Fazenda de Ensino, Pesquisa e Extensão, city of Selvíria, MS, Brazil) belonging to UNESP/FEIS. The sampling area has an average annual rainfall of 1,300 mm with an average temperature of 23.5 °C, climate type is AW, according to Köeppen. The soil is classified as dystrophic red Latosol, sandy clay loam texture (Embrapa 2013EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária (2013) Sistema brasileiro de classificação de solos. Vol. 1. Ed. EMBRAPA, Rio de Janeiro. 306p.).

The area where the farm is located had a great impact in the 1970s, and a large area had about 8.6 m deth of soil removed to be used in the construction of the dam of the Ilha Solteira Hydroelectric Power Plant and, with this, the soil horizons A and B were lost, as well as great part of the nutrients (Modesto et al. 2009Modesto PT, Scabora MH, Colodro G, Maltoni KL & Cassiolato AMR (2009) Alterações em algumas propriedades de um latossolo degradado com uso de lodo de esgoto e resíduos orgânicos. Revista Brasileira de Ciência do Solo 33: 1489-1498.).

In this way, samples were collected in two different areas. The first area, which had a direct impact due to soil removal for the construction of the dam (A1), shows Astronium fraxinifolium specimens that had spontaneous sprout after soil removal. The second area, which was not directly impacted by the construction of the dam (A2), is a place where the species was cultivated, obtaining all the necessary conditions for its initial growth and development.

This natural regeneration in the area occurred at the same time that the planting of the seedlings of this species was carried out in the non-degraded area, so that both populations are close to 30 years old. It should be emphasized that only the impact caused by the removal of the surface layers of the soil for the construction of the hydroelectric dam is being considered, and not impacts coming from other sources.

In all, 20 trees from each studied area were choosen for sampling.

Soil analysis

For the physical analysis, 10 undeformed samples were sampled from each study area, 5 of them collected at depths of 0–20 cm and 5 of 20–40 cm, using the volumetric ring method (Teixera et al. 2017). This analysis was performed at the Soil Physics Laboratory of Unesp Ilha Solteira.

The chemical analysis of the soil was performed at the Soil Fertility Laboratory of Unesp Ilha Solteira. For this analysis, 10 composite samples collected from 20–40 cm deep were collected, using the method described by Raij et al. (2001)Raij BV, Andrade JC & Cantarella H (2001) Análise química para avaliação da fertilidade de solos tropicais. Vol. 1. Ed. Instituto Agronômico, Campinas. 276p..

Stomatal density

To determine stomatal density, it was performed cuttings in the medial portion of the third leaflet of Astronium fraxinifolium leaves of each study area, and such cuts (rectangles of approximately 1 × 2 cm) were fixed on the glass slides with fast drying glue, ester of cyanoacrylate (Segatto et al. 2004Segatto FB, Bisognin DA, Benedetti M, Costa LC, Rampelotto MV & Nicoloso FT (2004) Técnica para o estudo de anatomia da epiderme foliar de batata. Ciência Rural 34: 1597-1601.). After total drying of the glue, the plant material was removed from the blade leaving only the impression of the abaxial leaf face. Afterwards, photographs were taken of the blades with the abaxial face impressions of each sample with a 40X magnification. The total number of stomata was counted in each image. Considering the scale bar (µm) expressed in each photograph, the total area of the photo was calculated in µm2, from which it was transformed into mm2, making it possible to estimate the number of stomata per mm2.

Specific leaf area

The analysis of the specific leaf area was performed with digitization of 10 leaflets of the trees collected by the leaf area scanner belonging to Analytical Development Company Limited. Afterwards, they were oven dried at 65 ºC (Gobbi et al. 2011Gobbi KF, Garcia R, Ventrella MC, Garcez Neto AF & Rocha GC (2011) Área foliar específica e anatomia foliar quantitativa do capim-braquiária e do amendoim-forrageiro submetidos a sombreamento. Revista Brasileira de Zootecnia 40: 1436-1444.) for 72 hours. The specific leaf area was calculated, which consists of the ratio between the leaf area (cm2) and the weight of the leaf dry mass (g).

Gas exchange analysis and carbono allocation

The liquid photosynthesis, stomatal conductance and the internal CO2 concentration in the sub-stomatic chamber were evaluated using a portable gas exchange device, Infra Red Gas Analyzer (IRGA) (Richardson et al. 2017Richardson F, Brodribb TJ & Jordan GJ (2017) Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand. Tree Physiology 37: 869-878.; Paixão et al. 2017Paixão AP, Furlani-Junior E , Hiraki SS, Machado LHMD, Camargos LS, Carvalho FT (2017) Crescimento, fotossíntese e atividade enzimática de genótipos de algodoeiro herbáceo submetidos ao Cloreto de Mepiquat. Cultura Agronômica 26: 540-553.); brand ADC BioScientific Ltd, model LC-Pro, it was set 1,000 µmol m-2 s-1 of photosynthetically active radiation (PAR), provided by LED lamps and 380 ppm CO2 and chamber temperature at 28 °C. A branch was separated from the plant and immediately afterwards, gas exchange and carbon allocation of three random leaflets were measured. It should be noted that the measurements were made on a sunny day at dawn in both areas, avoiding climatic interference in the data.

Total chlorophyll determination

Fresh leaf samples were collected from both study areas. The dosage of chlorophylls a and b was performed according to Hiscox & Israeltam (1979)Hiscox JD & Israeltam GF (1979) A method for the extraction chlorophyll from leaf tissue without maceration. Canadian Journal of Botany 57: 1332-1334.. The leaves were cut into thin strips (1 mm) in 50 mg samples. Three replicates of the assay were made for each sample. The plant material was placed in a test tube with 7 mL of DMSO (dimethyl sulfoxide), covered with glass beads and kept in water bath at 65 ºC for 30 minutes in the dark. After cooling at room temperature, the extract was read in spectrophotometer at 645 and 663 nm (Arnon 1949Arnon DI (1949) Copperenzymes in isolated chloroplasts. Polyphrenol oxidase in Beta vulgaris. Plant Physiol 24: 1-15.). The content of the pigments was obtained from the equations proposed by Arnon, as follow below:

C a µ g . m l 1 = ( 12.70 × A 663 ) ( 2.69 × A 645 )
C b µ g . m l 1 = ( 22.90 × A 645 ) ( 4 , 68 × A 663 )
C a + C b µ g . m l 1 = ( 20.20 × A 645 ) + ( 8.02 × A 663 )

* Data expressed as µg/g FW (micrograms per gram of fresh weight).

Extraction and quantification of nitrogen compounds, total carbohydrate and starch

To extract nitrogen compounds, total carbohydrate and starch it was used the method described by Bieleski Turner (1966)Bieleski RL & Turner NA (1966) Separation and estimation of amino acids in crude plants extracts by thin-layer electrophoresis and chromatography. Analytical Biochemistry 17: 278-293.. For each 1g of fresh material it was added 10 ml of MCW solution (60% methanol, 25% chloroform, 15% ml H2O). The material was well crushed, homogenized and then centrifuged. Then, 1 ml Chloroform + 1.5 ml H2O was added for each 4 ml supernatant recoverd. The solution recovered was kept for 24-hour in fridge for phase separation and the water-soluble phase was used for the analysis of amino acids and total soluble carbohydrates.

After the first extraction, it was added 0.1 N NaOH (at a ratio of 1:10, w/v) to the remaining pellet, which was resuspended and centrifuged, and then the supernatant was recovered and used for total soluble proteins quantification.

After protein extraction, it was added 30% perchloric acid (at a ratio of 1:10, w/v) to the remaining pellet, which was resuspended and centrifuged, and then the supernatant was recovered and used for starch quantification.

Total soluble amino acids were quantified according to Yemm Cocking (1955)Yemm EW & Cocking EC (1955) The determination of amino-acids with ninhydrin. Analyst 80: 209-214.; total soluble protein was quantified according to Bradford (1976)Bradford M (1976) A rapid and sensitive method for the quantification of microgam quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.; total soluble carbohydrate and starch was quantified according to Umbreit et al. (1957)Umbreit WW, Kingsley GR & Schaffter RR (1957) A colorimetric method for transaminase in sérum or plasma. Journal of Laboratory and Clinical Medicine 49: 454-459..

Nutritional analysis

The sampled leaves were washed with distilled water containing a little detergent and then rinsed with distilled water in successive portions to remove any impurity and detergents. Then the leaves were placed on absorbent paper.

The leaves were placed in perforated paper bags and then dried in a forced air circulation oven, with a temperature ranging from 65 to 70 ºC. After dried, they were milled using a stainless steel mill to avoid contamination of the sample mainly by iron, zinc and copper. The grinded samples were subjected through a 1 mm sieve. This sieved material was used to determine N, P, K, Ca, Mg, S, Cu, Fe, Mn and Zn contents according to Malavolta et al. (1997)Malavolta E, Vitti GC & Oliveira SA (1997) Avaliação do estado nutricional das plantas: princípios e aplicações, Vol. 1. Ed. Potafos, Piracicaba. 319p..

Statistical analysis

To quantify nitrogen compounds, total carbohydrates, starch, nutritional content, gas exchange and carbon allocation, the analyzes consisted of three random leaflets from each individual, among the 20 field trees we randomly sampled 6 to carry out the analysis aforementioned. For the analysis of chlorophyll, stomatal density and specific leaf area, 20 trees from each area were sampled and evaluated.

All data were submitted to descriptive statistics, using R Core Team software (2018R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at <https://www.R-project.org/>. Access on 24 April 2020.
https://www.R-project.org/...
), in order to evaluate the possible morphophysiological differences in plants of the different areas studied.

Results

Soil characteristics

The physical analysis of the soil showed that A1 and A2 present very different characteristics for the apparent density, macroporosity, microporosity and total porosity attributes (Tab. 1).

Table 1
Bulk density (BD), macroporosity (MA), microporosity (MI) and total porosity (PT) of soil A1 and A2, at depths of 0–20 cm and 20–40 cm.

The chemical characteristics of the soil that presented differences between the areas were: sum of bases (SB); aluminum saturation (m%); cation exchange capacity (C.E.C); organic matter content (MO). SB was 9.5 mmolc dm-3 for A13+ and 12.1 mmolc dm-3 for A2. For m%, an average of 43% was observed for A1 and 52% for A2. Soil C.E.C was 34.5 and 76.1 mmolc dm-3 for A1 and A2 respectively, with MO of 13 g dm-3 in A1 and 23 g dm-3 in A2. The soil in both areas is acidic, with values of 4.4 for A1 and 4.1 for A2.

Morphophysiology of plant leaves

The epidermis of the Astronium fraxinifolium leaf presents cells with curved walls and anomocytic stomata, which are observed on both sides of the leaf, which is therefore called amphistomatic (Muir 2015Muir CD (2015) Making pore choices: repeated regime shifts in stomatal ratio. Proceedings of the Royal Society B: Biological Sciences 282: 20151498.). In the abaxial epidermis there are stomata in great numbers throughout the leaf surface, which is almost completely composed of stomata and guard cells. On the adaxial side, stomata and guard cells are present only in regions closer to the rib. A total of 1,801.5 and 1,619.5 stomata/mm2 on the abaxial surface were observed for leaves coming from the areas A1 and A2 (p = 0.035; n = 20), respectively, with A1 being statistically different from A2.

Regarding the specific leaf area, no significant difference was observed between the populations, presenting a mean of 82.87 cm2/g for A2 and 77.66 cm2/g for A1 (p = 0.17; n = 20). Considering gas exchanges and carbon allocation, there was no significant difference between the areas for all variables: stomatal conductance, internal CO2 concentration in the sub-stomatic chamber, liquid photosynthesis and transpiration (Tab. 2). For chlorophyll analysis, significant differences were found for the three variables. Chlorophyll a, b and total chlorophylls were significantly higher in A2 (Tab. 3).

Table 2
Net photosynthesis (A - μmol CO2 m-2 s-1 ), transpiration (E - mmol H2O m-2 s-1 ), stomatal conductance (gS - mol H2O m-2 s-1 ) e internal concentration of CO2 (Ci - μmol CO2 mol m-2 s-1 ) in leaves of Astronium fraxinifolium area A1 and A2.
Table 3
Concentration of chlorophylls a and b and total chlorophylls (µg/gMF) in leaves of Astronium fraxinifolium from areas A1 and A2.

The mineral content of Astronium fraxinifolium leaves showed that there was no significant difference between the two populations for all macro and micronutrients, except for boron (B), which was significantly higher in A2, with an average of 27 mg/kg A2 and 17 mg/kg in A1 (Tab. 4). Concerning the data of nitrogen compounds, total soluble proteins, total carbohydrate and starch, also there were no significant differences (Tab. 5).

Table 4
Concentration of macro and micronutrientes in leaves of Astronium fraxinifolium in areas A1 and A2.
Table 5
Concentration of soluble amino acids, soluble proteins, total carbohydrate and starch (µmol/gMF) in leaves of Astronium fraxinifolium in areas A2 and A1.

Discussion

Soil characteristics

There is a close relationship between total porosity and bulk density, when density increases, total porosity decreases (Chen et al. 2014Chen G, Weil RR & Hill RL (2014) Effects of compaction and cover crops on soil least limiting water range and air permeability. Soil & Tillage Research 136: 61-69.), with high density being indicative of soil compaction (Rosa-Filho et al. 2009Rosa Filho G, Carvalho MP, Andreotti M, Montanari R, Binotti FFS & Gioia MT (2009) Variabilidade da produtividade da soja em função de atributos físicos de um latossolo vermelho distroférrico sob plantio direto. Revista Brasileira de Ciência do Solo 33: 283-293.). Total porosity is composed of microporosity (soil water volume) and macroporosity (soil aeration). With the reduction of pores in the soil, in addition to making aeration difficult, it hinders root penetration and water infiltration into the soil (Calonego et al. 2017Calonego JC, Raphael JPA, Rigon JPG, Oliveira Neto L & Rosolem CA (2017) Soil compaction management and soybean yields with cover cropsunder no-till and occasional chiseling. European Journal of Agronomy 85: 31-37.).

Bowen (1981)Bowen HD (1981) Alleviating mechanical impedance. In: Arkin GF, Taylor HM (ed) Modifying the root environment to reduce crop stress. American Society of Agricultural Engineers, St. Joseph. Pp.21-57. states that a soil with a density greater than or equal to 1.55 kg dm-3 already has compaction that can affect root growth. For agriculture, the ideal is that the soil has microporosity between 0.250 and 0.330 m3 m-3 and macroporosity 0.170 and 0.250 m3 m-3, with the ideal total porosity of 0.500 m3m-3 (Kiehl 1979Kiehl EJ (1979) Manual de edafologia: relações solo-planta. Vol. 1. Ed. Agronômica Ceres, Piracicaba. 262p.; Lima et al. 2007Lima CGR, Carvalho MP, Mello LMM & Lima RC (2007) Correlação linear e espacial entre a produtividade de forragem, a porosidade total e a densidade do solo de Pereira Barreto (SP). Revista Brasileira de Ciência do Solo 31: 1233-1244.).

Studies conducted in preserved Cerrado areas show that soils in this biome have values ​​close to or above those indicated for agriculture. Sena et al. (2017)Sena KN, Maltoni KL, Faria GA & Cassiolato AMR (2017) Organic carbon and physical properties in sandy soil after conversion from degraded pasture to Eucalyptus in the Brazilian Cerrado. Revista Brasileira de Ciência do Solo 41: e0150505., for example, observed 0.470 m3 m-3 of total porosity in a soil of a preserved Cerrado area. Oliveira et al. (2013)Oliveira JGR, Filho JT & Barbosa GMC (2013) Qualidade física do solo das trilhas do parque estadual do Cerrado - PR. Ciências Agrárias 34: 1715-1722. and Araújo et al. (2007)Araújo R, Goedert WJ & Lacerda MPC (2007) Qualidade de um solo sob diferentes usos e sob cerrado nativo. Revista Brasileira de Ciência do Solo 31: 1099-1108., who also evaluated preserved Cerrado soil, observed values ​​of 0.580 and 0.650 m3 m-3 respectively, for total porosity.

As observed in this research, the A1 presents lower values than those presented in conserved Cerrado soil and recommended for agriculture, presenting compacted soil.

The m% is high in both areas, considering that soils with m% greater than 50% are considered alic, containing huge amount of exchangeable aluminum (Ronquim 2010Ronquim CC (2010) Conceitos de fertilidade do solo e manejo adequado para as regiões tropicais. Vol. 1. Embrapa, Campinas. 26p.), low CEC and acidic pH, characteristics that are common in Cerrado soils (Haridasan 2008Haridasan M (2008) Nutritional adaptations of native plants of the cerrado biome in acid soils. Brazilian Journal of Plant Physiology 20: 183-195.; Skorupa et al. 2012Skorupa ALA, Guilherme LRG, Curi N, Silva CPC, Scolforo JRS & Marques JJGSM (2012) Propriedades de solos sob vegetação nativa em Minas Gerais: distribuição por fitosionomia, hidrografia e variabilidade espacial. Revista Brasileira de Ciência do Solo 36: 11-22.).

Morphophysiology of plant leaves

Chlorophylls play a key role in photosynthesis and are components of the antenna complex, light absorption, excitation of the Photosynthesis Reaction Center and water photoxidation (Taiz Zeiger 2009Taiz L & Zeiger E (2009) Fisiologia vegetal. Vol. 1. Ed. Artmed, Porto Alegre. 848p.). In the studies of Lima et al. (2004)Lima MGS, Lopes NF, Bacarin MA & Mendes CR (2004) Efeito do estresse salino sobre a concentração de pigmentos e prolina em folhas de arroz. Bragantia 63: 335-340. with Oryza sativa, Neves et al. (2009)Neves NR, Oliva MA, Cruz-Centeno D, Costa AC, Ribas RF & Pereira EG (2009) Photosynthesis and oxidative stress in the restinga plant species Eugenia uniflora L. exposed to simulated acid rain and iron ore dust deposition: potential use in environmental risk assessment. Science of the Total Environment 407: 3740-3745. with Eugenia uniflora, Massacci et al. (2008)Massacci A, Nabiev SM, Pietrosanti L, Nematov SK, Chernikova TN, Thor K & Leipner J (2008) Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiology Biochemistry 46: 189-195. with cotton (Gossypium sp.) and Jaleel et al. (2008)Jaleel CA, Manivannan P, Lakshmanan GMA, Gomathinayagam M & Panneerselvam R (2008) Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits. Colloids and Surfaces B: Biointerfaces 61: 298-303. with Catharanthus roseus who showed a decrease in chlorophyll when presented with different types of plant stress, a result similar to that observed for A. fraxinifolium.

It has been reported in several studies that photosynthetic rate changes in plants subjected to environmental stresses (Rashid et al. 2018Rashid MA, Andersen MN, Wollenweber B, Zhang X & Olesen JE (2018) Acclimation to higher VPD and temperature minimized negative effects on assimilation and grain yield of wheat. Agricultural and Forest Meteorology 248: 119-129.; Karimi Tavallali 2017Karimi S & Tavallali V (2017) Interactive effects of soil salinity and boron on growth, mineral composition and CO2 assimilation of pistachio seedlings. Acta Physiologiae Plantarum 9: 242.; Silva et al. 2017Silva S, Pinto G & Santos C (2017) Low doses of Pb affected Lactuca sativa photosynthetic performance. Photosynthetica 55: 50-57.; Silva & Arrebaça 2004Silva JM & Arrabaça MC (2004) Photosynthesis in the water-stressed C4 grass Setaria sphacelata is mainly limited by stomata with both rapidly and slowly imposed water déficits. Physiologia Plantarum 121: 409-420.), such observations could indicate that the photosynthetic capacity of the plant was affected by stress and that, possibly, the individuals of A1 would present low photosynthetic rate. However, there was no change in net photosynthesis between the two populations.

In the literature, there are species that under environmental impact present an increase in leaf area (Gobbi et al. 2011Gobbi KF, Garcia R, Ventrella MC, Garcez Neto AF & Rocha GC (2011) Área foliar específica e anatomia foliar quantitativa do capim-braquiária e do amendoim-forrageiro submetidos a sombreamento. Revista Brasileira de Zootecnia 40: 1436-1444.; Rad et al. 2011Rad MH, Assare MH, Banakar MH & Soltani M (2011) Effects of different soil moisture regimes on leaf area index, specific leaf area and water use efficiency in Eucalyptus (Eucalyptus camaldulensis Dehnh) under dry climatic conditions. Asian Journal of Plant Sciences 10: 294-300.), and in other species there is a decrease (Scalon et al. 2011Scalon SPQ, Mussury RM, Euzébio VLM, Kodama FM & Kissmann C (2011) Estresse hídrico no metabolismo e crescimento inicial de mudas de mutambo (Guazuma ulmifolia Lam.). Ciência Florestal 21: 655-662.; Machado et al. 2010Machado AV, Souza TV, Santos M & Paulilo MTS (2010) Response of a woody species from Atlantic rain forest, Hedyosmum brasiliense Mart. ex Miq. (Chloranthaceae), submitted to water stress. Journal of Botany 39: 1-13.; Maranho et al. 2006Maranho LT, Galvão F, Preussler KH, Muñiz GIB & Kuniyoshi YS (2006) Efeitos da poluição por petróleo na estrutura da folha de Podocarpus lambertii Klotzsch ex Endl., Podocarpaceae. Acta Botanica Brasilica 20: 615-624.; Alves et al. 2001Alves ES, Giusti PM, Domingos M, Saldiva PHN, Guimarães ET & Lobo DJA (2001) Estudo anatômico foliar do clone híbrido 4430 de Tradescantia: alterações decorrentes da poluição aérea urbana. Revista brasileira de Botânica 24: 567-576.), in addition it should be expected increase in leaf area in leaves of Astronium fraxinifolium as a way to compensate the low amount of chlorophyll.

However, such landings did not occur. Despite this, the species in general has a very high stomatal density, as observed in Miconia pycnoneura (Howard 1969Howard RA (1969) The ecology of an elfin forest in Puerto Rico, 8. Studies of stem growth and form and of leaf structure. Journal Arnold Arboretum 50: 225-267.). The change in stomatal density is observed in studies with other species, and may be caused by several types of environmental changes such as: water stress (Nemerkéri et al. 2018; Khan et al. 2010Khan AS, Allah SU & Sadique S (2010) Genetic variability and correlation among seedling traits of wheat (Triticum aestivum) under water stress. International Journal of Agriculture and Biology 12: 1814-9596.; Batista et al. 2010Batista LA, Guimarães RJ, Pereira FB, Carvalho GR & Castro EM (2010) Anatomia foliar e potencial hídrico na tolerância de cultivares de café ao estresse hídrico. Revista Ciência Agronômica 41: 475-481.; Grisi et al. 2008Grisi FA, Alves JD, Castro EM, Oliveira C, Biagiotti G & Melo LA (2008) Avaliações anatômicas foliares em mudas de café “catuaí” e “siriema” submetidas ao estresse hídrico. Ciência e Agrotecnologia 32: 1730-1736.), salt stress (Barbiere et al. 2019; Shabala et al. 2013Shabala S, Hariadi Y & Jacobsen SE (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. Journal of Plant Physiology 170: 906- 914.; Orsini et al. 2012Orsini F, Alnayef M, Bona S, Maggio A & Gianquinto G (2012) Low stomatal density and reduced transpiration facilitate strawberry adaptation to salinity. Environmental and Experimental Botany 81: 1-10), shading (Gobbi et al. 2011Gobbi KF, Garcia R, Ventrella MC, Garcez Neto AF & Rocha GC (2011) Área foliar específica e anatomia foliar quantitativa do capim-braquiária e do amendoim-forrageiro submetidos a sombreamento. Revista Brasileira de Zootecnia 40: 1436-1444.), pollution (Alves et al. 2008Alves ES, Tresmondi F & Longui EL (2008) Análise estrutural de folhas de Eugenia uniflora L. (Myrtaceae) coletadas em ambientes rural e urbano, SP, Brasil. Acta Botanica Brasilica 22: 241-248.; Maranho et al. 2006Maranho LT, Galvão F, Preussler KH, Muñiz GIB & Kuniyoshi YS (2006) Efeitos da poluição por petróleo na estrutura da folha de Podocarpus lambertii Klotzsch ex Endl., Podocarpaceae. Acta Botanica Brasilica 20: 615-624. ) and even the rise in altitude (Kučerová et al. 2018Kučerová J, Konôpková A, Pšidová E, Kurjak D, Jamnická G, Slugenová K, Gömöry D & Ditmarová L (2018) Adaptive variation in physiological traits of beech provenances in Central Europe. iForest - Biogeosciences and Forestry 11: 24-31.). Thus, it is believed that such characteristics are adaptations that allow the survival of the species under conditions of environmental stress, so that there is an increase in the number of stomata as a way to compensate the low production of photosynthetic pigments.

Thus, the fact that the plant does not need to invest heavily in chlorophyll production indicates that under such stress would be more likely to establish itself in the environment, using the few nutrients it can capture more effectively, since it is an expensive molecule to be produced by being composed of large amounts of carbon and nitrogen (Porra et al. 1994Porra RJ, Schäfer W, Cmiel E, Katheder I & Scheer H (1994) The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. European Journal of Biochemistry 219: 671-679.; Taiz Zeiger 2009Taiz L & Zeiger E (2009) Fisiologia vegetal. Vol. 1. Ed. Artmed, Porto Alegre. 848p.). This observation can be confirmed by the fact that there is no significant difference in the levels of nitrogen compounds, proteins, total carbohydrates and starch, so that this reflects the efficiency of nutrients utilization by the species.

Another change observed among populations was the concentration of boron in leaves, a factor that may be related to the characteristics of the soil. Boron, although not fully understood, is an essential nutrient for plants (Matoh Kobayashi 1998Matoh T & Kobayashi M (1998) Boron and Calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. Journal of Plant Research 111: 179-190.; Taiz Zeiger 2009Taiz L & Zeiger E (2009) Fisiologia vegetal. Vol. 1. Ed. Artmed, Porto Alegre. 848p.), and it is known that it has in important role in keeping the integrity of the cell wall, together with calcium (Cakmak Römheld 1997Cakmak I & Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193: 71-83.; Matoh Kobayashi 1998Matoh T & Kobayashi M (1998) Boron and Calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. Journal of Plant Research 111: 179-190.; Blevins Lukaszewski 1998Blevins DG & Lukaszewski KM (1998) Boron in plant structure and function. Annual Review of Plant Physiology and Plant Molecular Biology 49: 481-500.; Goldbach Wimmer 2007Goldbach HE & Wimmer MA (2007) Boron in plants and animals: is there a role beyond cell-wall structure? Journal of Soil Science and Plant Nutrition 170: 39-48.).

Thus, deficiency of this nutrient can cause problems in the integrity of the cell wall (Cakmak Römheld 1997Cakmak I & Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193: 71-83.) impairing root elongation (Dell Huang 1997Dell B & Huang L (1997) Physiological response of plants to low boron. Plant Soil 193: 103-120.), as well as cause anatomical changes in vascular tissues (Hajiboland et al. 2012Hajiboland R, Farhanghi F & Aliasgharpour M (2012) Morphological and anatomical modifications in leaf, stem and roots of four plant species under boron deficiency conditions. Anales de Biología 34: 15-29.). Also, boron deficiency may lead to decreased levels of chlorophylls and carotenoids (Moustafa-Farag et al. 2015Moustafa-Farag M, Sheng FB, Guy KM, Hu Z, Yang J & Zhang M (2015) Boron in watermelon i: activated antioxidant enzymes-reduced malondialdehyde concentration, and improved mineral uptakepromoted watermelon seedlings growth under boron deficiency. Journal of Plant Nutrition 39: 1989-2001.).

All these morphophysiological characteristics presented by the species allow it to be tolerant to environmental disturbance that it is exposed, so that it can survive and develop in a degraded soil (A1). This is corroborated by the fact that the species occurs by natural regeneration in A1 and does not present altered photosynthetic rate. Although there is a change in the chlorophyll content, we can infer that this factor is offset by an increase in stomatal abundance.

Observing all features, it is possible to emphasize the importance of the use of A. fraxinifolium for reforestation and recovery of degraded areas, since it is a pioneer plant species that survives under stressful environmental conditions for most species. It could not only reforest areas along with other species, but facilitating the establishment of early secondary species in the ecological succession process (Ferreira et al. 2010; Walker Wardle 2014Walker LR & Wardle DA (2014) Plant succession as an integrator of contrasting ecological time scales. Trends in Ecology & Evolution 29: 504-510.).

It can be inferred that the environmental stress, selects species with ability to adjust to the environment, so that these survive in different conditions, which can be observed in the species A. fraxinifolium.

We conclude that the decrease in boron content, the lower levels of chlorophylls and the increase in stomatal density can be an acclimation to the environmental changes to which the species has been exposed. These data confirm that A. fraxinifoluim presents great plasticity adapting the conditions of environmental stress. This fact is of extreme importance for studies of the recovery of degraded areas since it is a pioneer species and could be very used in the process of ecological succession of these areas.

Acknowledgements

The authors thanks the grant conceived by ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), the scholarship conceived to the second author, the support the publication of this paper (CAPES/AUXPE 88881.593505/2020-01) and the ‘Fundação de Amparo à Pesquisa do Estado de São Paulo’ for the scholarship for scientific initiation of the first author (n. 2017/00277-3)..

References

  • Alameda D & Villar R (2012) Linking root traits to plant physiology and growth in Fraxinus angustifolia Vahl. seedlings under soil compaction conditions. Environmental Experimental Botany 79: 49-57.
  • Alves ES, Giusti PM, Domingos M, Saldiva PHN, Guimarães ET & Lobo DJA (2001) Estudo anatômico foliar do clone híbrido 4430 de Tradescantia: alterações decorrentes da poluição aérea urbana. Revista brasileira de Botânica 24: 567-576.
  • Alves ES, Tresmondi F & Longui EL (2008) Análise estrutural de folhas de Eugenia uniflora L. (Myrtaceae) coletadas em ambientes rural e urbano, SP, Brasil. Acta Botanica Brasilica 22: 241-248.
  • Araújo FS, Martins SV, Meira Neto JAA, Lani JL & Pires IE (2006) Estrutura da vegetação arbustivo-arbórea colonizadora de uma área degradada por mineração de caulim, Brás Pires, MG. Revista Árvore 30: 107-116.
  • Araújo R, Goedert WJ & Lacerda MPC (2007) Qualidade de um solo sob diferentes usos e sob cerrado nativo. Revista Brasileira de Ciência do Solo 31: 1099-1108.
  • Aref IM, Ahmed AI, Khan PR, El-Atta HA & Iqbal M (2013) Drought-induced adaptive changes in the seedling anatomy of Acacia ehrenbergiana and Acacia tortilis subsp. raddiana Trees 27: 959- 971.
  • Arnon DI (1949) Copperenzymes in isolated chloroplasts. Polyphrenol oxidase in Beta vulgaris Plant Physiol 24: 1-15.
  • Barbieri GF, Stefanello R, Menegaes JF, Munareto, JD & Nunes UR (2019) Seed germination and initial growth of quinoa seedlings under water and salt stress. Journal of Agricultural Science 11: 153-161.
  • Batista LA, Guimarães RJ, Pereira FB, Carvalho GR & Castro EM (2010) Anatomia foliar e potencial hídrico na tolerância de cultivares de café ao estresse hídrico. Revista Ciência Agronômica 41: 475-481.
  • Bieleski RL & Turner NA (1966) Separation and estimation of amino acids in crude plants extracts by thin-layer electrophoresis and chromatography. Analytical Biochemistry 17: 278-293.
  • Blevins DG & Lukaszewski KM (1998) Boron in plant structure and function. Annual Review of Plant Physiology and Plant Molecular Biology 49: 481-500.
  • Bowen HD (1981) Alleviating mechanical impedance. In: Arkin GF, Taylor HM (ed) Modifying the root environment to reduce crop stress. American Society of Agricultural Engineers, St. Joseph. Pp.21-57.
  • Bradford M (1976) A rapid and sensitive method for the quantification of microgam quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
  • Cakmak I & Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193: 71-83.
  • Calonego JC, Raphael JPA, Rigon JPG, Oliveira Neto L & Rosolem CA (2017) Soil compaction management and soybean yields with cover cropsunder no-till and occasional chiseling. European Journal of Agronomy 85: 31-37.
  • Cambi M, Mariotti B, Fabiano F, Maltoni A, Tani A, Foderi C, Laschi A & Marchi E (2017) Early response of Quercus robur seedlings to soil compaction following germination. Land Degradation & Development 29: 916-925.
  • Cambi M, Hoshika Y, Mariotti B, Paoletti E, Picchio R, Venanzi R & Marchi E (2016) Compaction by a forest machine affects soil quality and Quercus robur L. seedling performance in an experimental field. Forest Ecology and Management 384: 406-414.
  • Campos JC & Landgraf PRC (2001) Análise da regeneração natural de espécies florestais em matas ciliares de acordo com a distância da margem do lago. Ciência Florestal 11: 143-151.
  • Chen G, Weil RR & Hill RL (2014) Effects of compaction and cover crops on soil least limiting water range and air permeability. Soil & Tillage Research 136: 61-69.
  • Costa VP, Hayashi AH, Carvalho MAM & Silva EA (2012) Aspectos fisiológicos, anatômicos e ultra-estruturais do rizoma de Costus arabicus L. (Costaceae) sob condições de déficit hídrico. Hoehnea 39: 125-137.
  • Dell B & Huang L (1997) Physiological response of plants to low boron. Plant Soil 193: 103-120.
  • De Long C, Cruse R & Wiener J (2015) The soil degradation paradox: compromising our resources when we need them the most. Sustainability 7: 866-879.
  • Deon RC, Zilli D, Brandelero G & Machado RG (2018) Compaction and water infiltration capacity of a cambisol by the traffic of machines and cattle trampling Ciência Agrícola 16: 77-84.
  • Dinis C, Surový P, Ribeiro N & Oliveira MRG (2015) The effect of soil compaction at different depths on cork oak seedling growth. New Forests 46: 235-246.
  • EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária (2013) Sistema brasileiro de classificação de solos. Vol. 1. Ed. EMBRAPA, Rio de Janeiro. 306p.
  • Fahn A & Cutler D (1992) Handbuch der pflanzen anatomie encyclopedia of plant anatomy Traité d’ Anatomie Végétale: Xerophytes. Vol. 1. Ed. Gebrüder Borntraeger, Berlin. 176p.
  • Ferreira WC, Botellho AS, Davide AC, Faria JMR & Ferreira DF (2010) Regeneração natural como indicador de recuperação de área degradada a jusante da usina hidrelétrica de Camargos, MG. Revista Árvore 34: 651-660.
  • Gama JRV, Botelho AS & Bentes-Gama MM (2002) Composição florística e estrutura da regeneração natural de floresta secundária de várzea baixa no estuário amazônico. Revista Árvore 26: 559-566.
  • Gobbi KF, Garcia R, Ventrella MC, Garcez Neto AF & Rocha GC (2011) Área foliar específica e anatomia foliar quantitativa do capim-braquiária e do amendoim-forrageiro submetidos a sombreamento. Revista Brasileira de Zootecnia 40: 1436-1444.
  • Goldbach HE & Wimmer MA (2007) Boron in plants and animals: is there a role beyond cell-wall structure? Journal of Soil Science and Plant Nutrition 170: 39-48.
  • Grisi FA, Alves JD, Castro EM, Oliveira C, Biagiotti G & Melo LA (2008) Avaliações anatômicas foliares em mudas de café “catuaí” e “siriema” submetidas ao estresse hídrico. Ciência e Agrotecnologia 32: 1730-1736.
  • Haridasan M (2008) Nutritional adaptations of native plants of the cerrado biome in acid soils. Brazilian Journal of Plant Physiology 20: 183-195.
  • Hajiboland R, Farhanghi F & Aliasgharpour M (2012) Morphological and anatomical modifications in leaf, stem and roots of four plant species under boron deficiency conditions. Anales de Biología 34: 15-29.
  • Higuchi P, Reis MGF, Reis GG, Pinheiro AL, Silva CT & Oliveira CHR (2006) Composição florística da regeneração natural de espécies arbóreas ao longo de oito anos em um fragmento de floresta estacional semidecidual, em Viçosa, MG. Revista Árvore 30: 893-904.
  • Hiscox JD & Israeltam GF (1979) A method for the extraction chlorophyll from leaf tissue without maceration. Canadian Journal of Botany 57: 1332-1334.
  • Howard RA (1969) The ecology of an elfin forest in Puerto Rico, 8. Studies of stem growth and form and of leaf structure. Journal Arnold Arboretum 50: 225-267.
  • Jaleel CA, Manivannan P, Lakshmanan GMA, Gomathinayagam M & Panneerselvam R (2008) Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits. Colloids and Surfaces B: Biointerfaces 61: 298-303.
  • Karimi S & Tavallali V (2017) Interactive effects of soil salinity and boron on growth, mineral composition and CO2 assimilation of pistachio seedlings. Acta Physiologiae Plantarum 9: 242.
  • Kiehl EJ (1979) Manual de edafologia: relações solo-planta. Vol. 1. Ed. Agronômica Ceres, Piracicaba. 262p.
  • Khan AS, Allah SU & Sadique S (2010) Genetic variability and correlation among seedling traits of wheat (Triticum aestivum) under water stress. International Journal of Agriculture and Biology 12: 1814-9596.
  • Kučerová J, Konôpková A, Pšidová E, Kurjak D, Jamnická G, Slugenová K, Gömöry D & Ditmarová L (2018) Adaptive variation in physiological traits of beech provenances in Central Europe. iForest - Biogeosciences and Forestry 11: 24-31.
  • Lima CGR, Carvalho MP, Mello LMM & Lima RC (2007) Correlação linear e espacial entre a produtividade de forragem, a porosidade total e a densidade do solo de Pereira Barreto (SP). Revista Brasileira de Ciência do Solo 31: 1233-1244.
  • Lima MGS, Lopes NF, Bacarin MA & Mendes CR (2004) Efeito do estresse salino sobre a concentração de pigmentos e prolina em folhas de arroz. Bragantia 63: 335-340.
  • Lu P, Chacko EK, Bithell SL, Schaper H, Wiebel J, Cole S & Muller WJ (2012) Photosynthesis and stomatal conductance of five mango cultivars in the seasonally wet-dry tropics of northern Australia. Scientia Horticulturae 138: 108-119.
  • Lorenzi H (2002) Árvores Brasileiras. 4th ed. Ed. Instituto Plantarum, Nova Odessa. 368p.
  • Machado AV, Souza TV, Santos M & Paulilo MTS (2010) Response of a woody species from Atlantic rain forest, Hedyosmum brasiliense Mart. ex Miq. (Chloranthaceae), submitted to water stress. Journal of Botany 39: 1-13.
  • Malavolta E, Vitti GC & Oliveira SA (1997) Avaliação do estado nutricional das plantas: princípios e aplicações, Vol. 1. Ed. Potafos, Piracicaba. 319p.
  • Marangon LC, Soares JJ, Feliciano ALP & Silva e Brandão CFL (2008) Regeneração natural em um fragmento de floresta estacional semidecidual em Viçosa, Minas Gerais. Revista Árvore 32: 183-191.
  • Maranho LT, Galvão F, Preussler KH, Muñiz GIB & Kuniyoshi YS (2006) Efeitos da poluição por petróleo na estrutura da folha de Podocarpus lambertii Klotzsch ex Endl., Podocarpaceae. Acta Botanica Brasilica 20: 615-624.
  • Massacci A, Nabiev SM, Pietrosanti L, Nematov SK, Chernikova TN, Thor K & Leipner J (2008) Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiology Biochemistry 46: 189-195.
  • Matoh T & Kobayashi M (1998) Boron and Calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. Journal of Plant Research 111: 179-190.
  • Modesto PT, Scabora MH, Colodro G, Maltoni KL & Cassiolato AMR (2009) Alterações em algumas propriedades de um latossolo degradado com uso de lodo de esgoto e resíduos orgânicos. Revista Brasileira de Ciência do Solo 33: 1489-1498.
  • Moustafa-Farag M, Sheng FB, Guy KM, Hu Z, Yang J & Zhang M (2015) Boron in watermelon i: activated antioxidant enzymes-reduced malondialdehyde concentration, and improved mineral uptakepromoted watermelon seedlings growth under boron deficiency. Journal of Plant Nutrition 39: 1989-2001.
  • Muir CD (2015) Making pore choices: repeated regime shifts in stomatal ratio. Proceedings of the Royal Society B: Biological Sciences 282: 20151498.
  • Nameskéri E, Molnár K, Pék Z & Helyes L (2018) Effect of water supply on the water use-related physiological traits and yield of snap beans in dry seasons. Irrigation Science 36: 143-158.
  • Neri AV, Campos EP, Duarte TG, Meira Neto JAA, Silva AF & Valente GE (2005) Regeneração de espécies nativas lenhosas sob plantio de Eucalyptus em área de Cerrado na Floresta Nacional de Paraopeba, MG, Brasil. Acta Botanica Brasilica 19: 369-376.
  • Neves NR, Oliva MA, Cruz-Centeno D, Costa AC, Ribas RF & Pereira EG (2009) Photosynthesis and oxidative stress in the restinga plant species Eugenia uniflora L. exposed to simulated acid rain and iron ore dust deposition: potential use in environmental risk assessment. Science of the Total Environment 407: 3740-3745.
  • Oliveira JGR, Filho JT & Barbosa GMC (2013) Qualidade física do solo das trilhas do parque estadual do Cerrado - PR. Ciências Agrárias 34: 1715-1722.
  • Orsini F, Alnayef M, Bona S, Maggio A & Gianquinto G (2012) Low stomatal density and reduced transpiration facilitate strawberry adaptation to salinity. Environmental and Experimental Botany 81: 1-10
  • Paixão AP, Furlani-Junior E , Hiraki SS, Machado LHMD, Camargos LS, Carvalho FT (2017) Crescimento, fotossíntese e atividade enzimática de genótipos de algodoeiro herbáceo submetidos ao Cloreto de Mepiquat. Cultura Agronômica 26: 540-553.
  • Porra RJ, Schäfer W, Cmiel E, Katheder I & Scheer H (1994) The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. European Journal of Biochemistry 219: 671-679.
  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at <https://www.R-project.org/>. Access on 24 April 2020.
    » https://www.R-project.org/
  • Rad MH, Assare MH, Banakar MH & Soltani M (2011) Effects of different soil moisture regimes on leaf area index, specific leaf area and water use efficiency in Eucalyptus (Eucalyptus camaldulensis Dehnh) under dry climatic conditions. Asian Journal of Plant Sciences 10: 294-300.
  • Raij BV, Andrade JC & Cantarella H (2001) Análise química para avaliação da fertilidade de solos tropicais. Vol. 1. Ed. Instituto Agronômico, Campinas. 276p.
  • Rashid MA, Andersen MN, Wollenweber B, Zhang X & Olesen JE (2018) Acclimation to higher VPD and temperature minimized negative effects on assimilation and grain yield of wheat. Agricultural and Forest Meteorology 248: 119-129.
  • Richardson F, Brodribb TJ & Jordan GJ (2017) Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand. Tree Physiology 37: 869-878.
  • Ronquim CC (2010) Conceitos de fertilidade do solo e manejo adequado para as regiões tropicais. Vol. 1. Embrapa, Campinas. 26p.
  • Rosa Filho G, Carvalho MP, Andreotti M, Montanari R, Binotti FFS & Gioia MT (2009) Variabilidade da produtividade da soja em função de atributos físicos de um latossolo vermelho distroférrico sob plantio direto. Revista Brasileira de Ciência do Solo 33: 283-293.
  • Scalon SPQ, Mussury RM, Euzébio VLM, Kodama FM & Kissmann C (2011) Estresse hídrico no metabolismo e crescimento inicial de mudas de mutambo (Guazuma ulmifolia Lam.). Ciência Florestal 21: 655-662.
  • Sena KN, Maltoni KL, Faria GA & Cassiolato AMR (2017) Organic carbon and physical properties in sandy soil after conversion from degraded pasture to Eucalyptus in the Brazilian Cerrado. Revista Brasileira de Ciência do Solo 41: e0150505.
  • Shabala S, Hariadi Y & Jacobsen SE (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. Journal of Plant Physiology 170: 906- 914.
  • Segatto FB, Bisognin DA, Benedetti M, Costa LC, Rampelotto MV & Nicoloso FT (2004) Técnica para o estudo de anatomia da epiderme foliar de batata. Ciência Rural 34: 1597-1601.
  • Silva S, Pinto G & Santos C (2017) Low doses of Pb affected Lactuca sativa photosynthetic performance. Photosynthetica 55: 50-57.
  • Silva JM & Arrabaça MC (2004) Photosynthesis in the water-stressed C4 grass Setaria sphacelata is mainly limited by stomata with both rapidly and slowly imposed water déficits. Physiologia Plantarum 121: 409-420.
  • Skorupa ALA, Guilherme LRG, Curi N, Silva CPC, Scolforo JRS & Marques JJGSM (2012) Propriedades de solos sob vegetação nativa em Minas Gerais: distribuição por fitosionomia, hidrografia e variabilidade espacial. Revista Brasileira de Ciência do Solo 36: 11-22.
  • Taiz L & Zeiger E (2009) Fisiologia vegetal. Vol. 1. Ed. Artmed, Porto Alegre. 848p.
  • Teixeira PC, Donagemma GK, Fontana A & Teixeira WG (2017) Manual de Métodos de Análise de Solo. Vol. 1. Ed. EMBRAPA, Brasília. 574p.
  • Umbreit WW, Kingsley GR & Schaffter RR (1957) A colorimetric method for transaminase in sérum or plasma. Journal of Laboratory and Clinical Medicine 49: 454-459.
  • Venturoli F, Felfili JM & Fagg CW (2011) Avaliação temporal da regeneração natural em uma floresta estacional semidecídua secundária, em Pirenópolis, Goiás. Revista Árvore 35: 473-483.
  • Walker LR & Wardle DA (2014) Plant succession as an integrator of contrasting ecological time scales. Trends in Ecology & Evolution 29: 504-510.
  • Wang L, Chang J, Zheng X, Liu J, Yu M, Liu L, Yang Y & Zhang H (2018) Survey of ecological environmental conditions and influential factors for public parks in Shanghai. Chemosphere 190: 9-16.
  • Warren CR, Aranda I & Cano FJ (2011) Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant, Cell & Environment 34: 1609-1629.
  • Yemm EW & Cocking EC (1955) The determination of amino-acids with ninhydrin. Analyst 80: 209-214.

Publication Dates

  • Publication in this collection
    20 Sept 2021
  • Date of issue
    2021

History

  • Received
    27 Apr 2020
  • Accepted
    05 Aug 2020
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