Effects on plant physiology in response to inoculation of growth-promoting bacteria: systematic reviewAbstract
Changes in physiological mechanisms resulting from the association of plant growth-promoting bacteria as well as the responses generated to stressful factors are of interest for sustainable agriculture. Based on this, the objective of this study was to gather insights from recent years (2012-2022) on the impacts on plant physiology of the use of inoculants from plant growth-promoting bacteria. To do this, the search for articles was done in three different databases, Science Direct, Springer Nature and Google Scholar, using the following descriptors: plant growth promoting bacteria, plant hormones, biological control, photosynthesis and abiotic stress. After selection, the included articles were systematized in the Excel program. Pearson Correlation and Principal Component Analysis were used for comparative analysis of physiological variables. 81 articles were included in the review, where a beneficial association was observed in 45 plant species distributed in 13 Orders and 13 Families, with emphasis on the Families Poaceae, Fabaceae, Solanaceae and Brassicaceae. 47 genera and 98 bacterial species were verified, where Bacillus and Pseudomonas represented 52% of the verified strains, with emphasis on Bacillus subtilis and Pseudomonas fluorescens. The main applications were growth promotion, productivity, control of biotic stress and abiotic stress. Positive regulation of photosynthesis was observed, modulating the gene expression of photosynthetic apparatus proteins, pigments, antioxidant production, increased hormonal and nutritional production, osmolyte content, antimicrobial production and decreased lipid peroxidation. Based on this review, it was possible to understand the multifaceted role of plant growth-promoting bacteria in contributing to the better direction of technology in agriculture.
Keywords:
sustainable agriculture; plant growth promotion; Bacillus; Pseudomonas
Resumo
Mudanças nos mecanismos fisiológicos decorrentes da associação de bactérias promotoras de crescimento vegetal, bem como as respostas geradas a fatores estressantes, são de interesse para a agricultura sustentável. Com base nisso, o objetivo deste estudo foi reunir informações dos últimos anos (2012-2022) sobre os impactos na fisiologia vegetal causados pelo uso de inoculantes de bactérias promotoras de crescimento vegetal. Para isso, a busca de artigos foi feita em três bases de dados diferentes: Science Direct, Springer Nature e Google Scholar, utilizando os seguintes descritores: bactérias promotoras de crescimento de plantas, hormônios vegetais, controle biológico, fotossíntese e estresse abiótico. Após seleção, os artigos incluídos foram sistematizados no programa Excel. Correlação de Pearson e Análise de Componentes Principais foram utilizadas para análise comparativa das variáveis fisiológicas. Foram incluídos 81 artigos na revisão, em que se observou associação benéfica em 45 espécies vegetais distribuídas em 13 Ordens e 13 Famílias, com destaque para as Famílias Poaceae, Fabaceae, Solanaceae e Brassicaceae. Foram verificados 47 gêneros e 98 espécies bacterianas, em que Bacillus e Pseudomonas representaram 52% das cepas verificadas, com destaque para Bacillus subtilis e Pseudomonas fluorescens. As principais aplicações foram promoção de crescimento, produtividade, controle de estresse biótico e estresse abiótico. Foi observada regulação positiva da fotossíntese, modulando a expressão gênica de proteínas do aparelho fotossintético, pigmentos, produção de antioxidantes, aumento da produção hormonal e nutricional, conteúdo de osmólitos, produção de antimicrobianos e diminuição da peroxidação lipídica. Com base nesta revisão, foi possível compreender o papel multifacetado das bactérias promotoras do crescimento das plantas na contribuição para o melhor direcionamento da tecnologia na agricultura.
Palavras-chave:
agricultura sustentável; promoção do crescimento vegetal; Bacillus; Pseudomonas
1. Introduction
The use of inoculants in agriculture results in economic and environmental impacts for the global population. The increase in agricultural productivity in line with the reduction in the use of chemical inputs is considered one of the greatest gains in modern agriculture, generated by this technology. In 2022, the global market for agricultural inoculants reached US$ 1.1 billion, and could reach US$ 1.7 billion by 2027 (Market and Markets, 2023). In Brazil, the biological inputs market is growing rapidly, according to the Associação Nacional dos Produtores e Importadores de Inoculantes (ANPII), the country sold 90 million doses of inoculants in the 2022 harvest (Oliveira et al., 2022).
The search for new potential strains for the formulation of these bioinputs is constant. The synergistic interaction between microorganism and host stimulates local and systemic responses in the plant through signaling and modulation of various molecular and cellular mechanisms. As a consequence, plants acquire levels of tolerance when imposed on environmental stresses, such as drought, high radiation, high temperatures, pests and diseases (Rozpądek et al., 2019; Qiang et al., 2019).
The effects of plant growth-promoting bacteria (PGP) are presented through direct and indirect mechanisms depending on their involvement in plant metabolism. Biological nitrogen fixation, solubilization of soil nutrients, the production of plant hormones, siderophores and the biological control of pathogenic agents through lytic enzymes such as cellulases, chitinases, lipases and proteases are some examples of these mechanisms (Etesami and Maheshwari, 2018; Rehman et al., 2020)
Plants will always be subject to biotic and abiotic interference, which can lead to possible stress. Therefore, the technology of using inoculants formulated from bacteria that promote plant growth has contributed to the development of more tolerant and productive plants. Therefore, understanding the physiological mechanisms resulting from the bacteria/host association, as well as the responses generated to stressful factors, brings important information to the scientific community, especially how PGP interferes with plant metabolism. Therefore, this is a systematic review that aims to gather information on the effects and changes in plant physiology through the use of plant growth-promoting bacteria (PGP).
2. Material and Methods
This is a systematic review on the effects on plant physiology resulting from the inoculation of growth-promoting bacteria. This review was written based on the guidelines proposed in the Preferred Reporting Intems for Systematic Reviews and MetaAnalyses (PRISMA) guide (Moher et al., 2015; Shamseer et al., 2015).
The search for articles was done in three different databases, Science Direct, Springer Nature and Google Scholar, which were identified by the following descriptors plant growth promoting bacteria, plant hormones, biological control, photosynthesis, and abiotic stress. Articles published in English between 2012 and 2022 were used in this review. The inclusion criteria for the articles were: (1) research articles, (2) application of bacteria as pure culture or formulation, (3) analyzes of the effect of bacteria on plant metabolism. Regarding the exclusion criteria, the articles considered inappropriate were: (1) review articles or book chapters, (2) studies with microorganisms other than bacteria, (3) studies with exclusively in vitro analyses, (4) evaluation only of morphological characters after inoculation.
The inclusion or exclusion of articles was done by reading titles and abstracts, where the included articles were saved for later analysis of results. Subsequently, the articles were systematized in the Excel program, to separate information regarding the plant and bacterial species studied, use of pure culture or formulation, effects on the plant and author/year of publication. Subsequently, this information was organized into tables and figures in order to obtain a comparative analysis.
Pearson's correlation was used to measure the statistical relationship between physiological variables, using the GraphPad Prism 9.5 program. Principal Component Analysis (PCA) was used to analyze the interrelationships between physiological variables and bacterial genera identified in the studies.
3. Results
After searching for articles using the descriptors presented, a total of 19,810 records were obtained, distributed as follows: 17,300 in the Google Scholar database, 1,680 obtained in Science Direct and 830 obtained in the Springer Nature database (Figure 1). Among the records found, titles and abstracts were first read, and 428 articles were included. After reading, 309 articles were discarded because they did not meet the inclusion criteria, leaving 119 articles. Duplicate articles were subsequently excluded, totaling 81 articles included in the systematic review (Figure 1).
Flowchart of article selection on the applications of plant growth-promoting bacteria (PGP) in agriculture and their effects on plant physiology.
A gradual increase has been observed over the years in the use of PGP bacteria in agriculture. Figure 2A reveals a marked progression between the years 2012 and 2022. It can be seen that the majority of studies were developed in the last 3 years (2020-2022), which together represent 51.9% of the articles. Figure 2B shows the continents that most develop studies on this topic, with the Asian continent in first place, where India is the prominent country (Table 1).
Temporal and geographic distribution of studies. (A) Percentage of articles identified by year of publication; (B) Geographic distribution of selected article
Geographic distribution of studies on PGP bacteria applications in agriculture and their effects on plant physiology, by continent and country.
According to Figure 3A, 45 plant species were identified in this study, divided into 13 Orders and 13 Families (Figure 3A). Higher frequencies of species from the Families Poaceae, Fabaceae, Solanaceae and Brassicaceae were found, with Zea mays (corn), Glycine max (soybean), Solanum lycopersicum (tomato) and Arabidopsis thaliana (starweed) being the most worked species within each Family, respectively (Figure 3B, 3C, 3D, 3E).
Plant families and species associated withplant growth-promoting bacteria (PGP). (A) Percentage of articles by plant species; (B) Percentage of articles by species of the Poaceae family; (C) Percentage of articles by species of the Fabaceae family; (D) Percentage of articles by species of the Fabaceae family; (E) Percentage of articles by species of the Brassicaceae family.
In total, 98 bacterial species (163 strains) belonging to 47 genera were identified, creating beneficial associations with plants. It was found that out of 163 strains studied, 85 of them are from the genera Bacillus (35.5%) and Pseudomonas (16.5%), both representing 52% of the strains analyzed across the studies (Figure 4A). For the genus Bacillus, 58 strains were identified in 44 articles (54.3%), with Bacillus subtilis the most studied species currently (Figure 4B). For the genus Pseudomonas, 27 strains were identified in 20 articles (24.7%), with Pseudomonas fluorescens the most discussed species within this genus, and the second most studied currently (Figure 4C). Other genera were highlighted, such as Paenibacillus (5.7%), Enterobacter (4.5%), Serratia (3.4%), Streptomyces (3.4%), Azospirillum (3.4%), Achromobacter (3.4%) and Herbaspirillum (3.4%) (Figure 4A).
Most frequent bacterial genera and species among the articles. (A) Most frequent genres by articles; (B) Frequency of Bacillus species; (C) Frequency of Pseudomonas species.
The main applications and benefits generated by plants, when combined with PGPs, were growth promotion, productivity, control of biotic stress (diseases) and abiotic stress (water, saline, metals, heat and others). It is noted that there is a high trend of research aimed at promoting plant growth and controlling salt stress. These biostimulant effects, together, represent 55.1% of the content covered among the articles (Figure 5A). Furthermore, out of eight biostimulant implications, the genera Bacillus and Pseudomonas stood out, exhibiting eight and seven of the effects, respectively (Figure 5B).
Biostimulant effects promoted using plant growth-promoting bacteria (PGP). (A) Frequency of articles by biostimulatory effect; (B) Relationship between the main bacterial genera and their biostimulant effects.
In general, bacterial inoculation has demonstrated positive regulation in metabolism, modulating the gene expression of photosynthetic apparatus proteins, pigments, antioxidant production, increased hormonal and nutritional production, osmolyte content, antimicrobial production and decreased lipid peroxidation, consequently reflecting on the adaptation of plants to environmental stress.
The physiological effects have been analyzed by numerous scientific methods. To analyze implications related to gas exchange and water use efficiency, the variables evaluated were photosynthesis (A), transpiration (E), stomatal conductance (Gs), water use efficiency (WEU) and carboxylation efficiency (EC). Chlorophyll fluorescence measurements were also addressed as current quantum efficiency (ΔF/Fm'), potential quantum efficiency (Fv/Fm) of photosystem II (PSII), photochemical quenching (qP), non-photochemical quenching (NPQ) and electron flow in PSII (ETR) (Supplementary Material).
Biochemical analysis under parameters of nutritional, enzymatic, hormonal and defense metabolism were addressed. Due to environmental stress, there is a constant threat to the conformational stability of intracellular proteins, thus the production of molecules that done cellular homeostasis such as osmolytes (proline, glycine and betaine) and antioxidant enzymes (SOD, CAT, APX, GR, GPOX, POX and GS) were detected between studies (Supplementary Material). The reduction of lipid peroxidation, expression of process regulatory genes (ZmGR1, ZmAPX1, ZmNHX3 and ZmWRKY58) and production of antimicrobial substances (siderophores, hydrogen cyanide-HCN, flavonoids, salicylic acid, phytoalexins and VOCs) are also other variables positively regulated after inoculation (Supplementary Material).
The Pearson correlation for physiological variables affected in responses to inoculation is shown in Figure 6. The more intense the shade of blue, the stronger the correlation between the variables (Figure 6). It is noted that all variables showed a positive correlation, only the intensity varied. Correlations above 0.9 are considered very strong, such as photosynthesis x stomatal conductance and pigments x nutrition (Figure 6). Between 0.7 to 0.9 indicates a strong correlation, such as gene regulation x nutrition and antimicrobials x photosynthesis. Values 0.5 to 0.7 indicate a moderate correlation, for example we have hormones x antimicrobials and lipid peroxidation x photosynthesis. Few weak correlations were presented (0.3 to 0.5), but hormone x nutrition and proline x hormone are some examples. No negative correlation was identified (Figure 6).
Pearson correlation (p) of physiological variables in response to plant growth-promoting bacteria (PGP).
The Principal Component Analysis (Figure 7) of the data set containing all physiological characters related to bacterial genera accumulated 82.4% in accumulated variation therefore explaining a large part of the data variability (above 50%).
4. Discussion
In recent years, modern agriculture, with conservationist characteristics, has focused on developing sustainable technologies to increase production without causing impacts to the ecosystem. Therefore, the use of biological inputs in agriculture, such as the use of beneficial bacteria, has been a technique that has demonstrated numerous benefits to crops and is used as an alternative to complying with the UN 2030 Agenda, which includes the Sustainable Development Goals (Dubey et al., 2022; Elnahal et al., 2022).
In this sense, the Asian continent has advanced with representative scientific contributions in the discovery of new strains with biostimulant potential. This fact corroborates the findings of this study, in which 60.4% of the articles were developed by Asian countries. It is important to highlight that this continent has 4.5 billion people (60.3% of the global population), in addition to being responsible for 50% of agricultural production, with annual growth of 3.8% (Wyckhuys et al., 2020). Furthermore, agriculture not only provides food, but also raw materials that supply large industries in the region, making agriculture a powerful engine of economic development (Wyckhuys et al., 2020).
Brazil was the 4th country with the highest percentage of studies with, representing 9.8% of published articles. We should highlight that Brazil is the 4th largest food producer in the world and a highlight in research and commercialization of inoculants. According to the Associação Nacional dos Produtores e Importadores de Inoculantes (ANPII, 2022), inoculant sales exceed the 90 million dose mark, becoming a key strategy for the country, where the majority of fertilizers used in agriculture are imported (Oliveira et al., 2022).
Among the Families with the largest number of species worked, Poaceae, Fabaceae, Solanaceae and Brassicaceae stand out. Poaceae, or also called Gramineae, is the fourth largest family of flowering plants, with around 11,000 species in almost 800 genera worldwide, being considered the most important for human consumption (Peterson, 2013; Soreng et al., 2015). In this context, researchers consider species from the Poaceae family as important hosts for inoculants, where numerous studies have reported improvements in productive performance, such as early tillering and better reproductive performance in rice (Doni et al., 2022), grain filling rate and the grain weight per corn plant (Alori et al., 2019), improvement in the concentration of mineral nutrients and an increase in yield of up to 17% in wheat (Hussain et al., 2020).
As for the Fabaceae, Solanaceae and Brassicasseae Families, some representative species stood out, such as soybean, tomato and starwort, respectively. Soybeans are among the main commodities, playing a fundamental role in the security of the global food supply with an equivalent production of 355.5 million tons cultivated on 130.9 million hectares (Embrapa, 2022). It has been shown to be the ideal crop for the use of inoculants due to the biological nitrogen fixation (BNF) process, resulting in nitrogen supply rates greater than 80%, with high grain yield (Zilli et al., 2021). The savings in the use of mineral nitrogen promoted by the use of inoculants already reach a value of more than US$ 13 billion (Hungria and Mendes, 2015).
Tomato is one of the most popular and cultivated vegetables in the world, but it is an extremely sensitive crop to more than 200 diseases caused by a variety of phytopathogenic microorganisms (Shahid et al., 2022). This fact has contributed to the increase in studies on the species, mainly focused on the biological control of diseases using bacterial inoculants. Studies point to several specific mechanisms used by strains in control, such as antibiosis, competition, production of cellulolytic enzymes, cyanogenic compounds, siderophores and induced systemic resistance (Dimkić et al., 2022; Elnahal et al., 2022).
The species Arabidopsis thaliana, known as starwort, or also as a model plant, is a valuable angiosperm for research in plant physiology, biochemistry and development. Researchers point to it as a model to address fundamental questions of the function and biological structure common to eukaryotes, such as regulatory metabolic routes, genetic approaches, as well as response to the effects produced from bacterial inoculation, to generate rapid returns, as it is a short-cycle plant (Delatorre and Silva, 2008; Meinke et al., 1998).
Bacillus and Pseudomonas represented 52% of the strains analyzed betweeen studies. Bacillus is a representative of gram-positive bacteria, and is currently the most used in the biological inoculant market, due to its easy colonization in plants and ability to produce durable formulations due to the formation of endospores (Borriss, 2015). Furthermore, it is a microorganism that can be easily cultivated in the laboratory, and can be isolated from different substrates such as soil organic matter, rhizosphere, endophyte (Sansinenea, 2019). The literature addresses improvements in plant health and productivity, which are mediated by three ecological mechanisms: production of antimicrobials against pathogenic organisms, secretion of compounds that promote plant growth, whether under normal conditions or under abiotic stresses, and induction of systemic resistance (Kour et al., 2020).
Of 21 Bacillus species verified in the study, B. subtilis is the most studied species. It is a species with broad adaptability and synergistic interactions with a wide variety of hosts. Strains of B. subtilis have shown improvements in the availability of nutrients, mainly nitrogen, phosphorus and iron, which occur in the soil in a form inaccessible to plants. Furthermore, it is capable of altering the homeostasis of plant hormones, promoting cell division and consequent plant growth. Tolerance to environmental stresses, such as drought, has also been reported, as B. subtilis has been shown to be efficient in regulating biosynthesis genes for abscisic acid, one of the main plant hormones for stress regulation (Woo et al., 2020; Blake et al., 2021).
Pseudomonas is another prominent genus, where 13 different species presented biostimulant characteristics, with emphasis on Pseudomonas fluorescens. In nature, this genus encompasses more than 250 species, predominantly in the rhizosphere. It presents a rapid growth rate, high metabolic versatility, developing control of biotic and abiotic stress by modulating the concentrations of 1-aminocyclopropane-1-carboxylate (ACC) deaminase in the plant, this is because the gene that encodes ACC deaminase (acdS) is present in 2,591 Pseudomonas genomes, being fundamental for bacteria-plant interaction by reducing the level of ethylene produced by the plant (Glick and Nascimento, 2021).
Pseudomonas fluorescens is studied mainly for biological control due to the suppression of pathogens such as Ralstonia solanacearum (tomato wilt), Clavibacter michiganensis subsp. michiganensise (tomato wilt), Monographella albescens (rice leaf scald), one of the main mechanisms being the induction of ROS scavenging enzymes such as peroxidase (POX), polyphenol oxidase (PPO) and lipoxygenase (LOX) (Abo-elyousr et al., 2019; Bueno et al., 2017; Suresh et al., 2022). The production of phenolic compounds, flavonoids and phytoalexins are also important mechanisms of this species to inhibit the development of pathogens (Chiappero et al., 2019; Sahebani and Gholamrezaee, 2021).
Plant growth promotion is the main effect found in plants associated with bacterial inoculants, where 31% of studies addressed biostimulant and biofertilizer effects. In this work, the vegetative and reproductive changes of plants are perceived mainly by the improvement in the nutritional aspects of the plant, providing fixed nitrogen through biological nitrogen fixation, phosphorus through phosphate solubilization, in addition to potassium, calcium, magnesium, zinc, iron, among other essential minerals (Basu et al., 2021). Much of the soil's nutrients may be unavailable, as they are linked to organic and inorganic constituents or present as insoluble precipitates. Therefore, the association may result in the transformation of compounds into their assimilable forms and releasing them into the soil solution, such as boron (H3BO3); copper (Cu2+); molybdenum (MoO42-), potassium (K+), zinc (Zn2+) magnesium (Mg2+) (Ramos et al., 2020). Higher nutrient contents resulted in greater fruit weight, greater aerial part and root diameter, greater fresh and dry mass, and greater productivity (Karlidag et al., 2007).
When it comes to promoting plant growth by bacteria, endogenous regulation of the levels of phytohormones such as auxins, cytokinins, gibberellins, abscisic acid and ethylene were one of the main aspects evaluated to analyze possible biostimulant effects among the articles. An aspect frequently discussed in the articles is the functioning of the ACC deaminase enzyme, reducing ethylene levels, facilitating plant growth, especially in the presence of abiotic and biotic stresses. Furthermore, the auxin, indole acetic acid (IAA), when secreted by bacteria, joins the IAA secreted by the plant, inducing cell proliferation or even inducing the transcription of genes for the production of ACC deaminase (Glick, 2020). In addition, to the synthesis of enzymes and hormones, other compounds with antimicrobial activity are detected in the bacteria-plant association response, such as siderophores, HCN, VOCs, isoprenes, flavonoids, salicylic acid and phytoalexins, forming part of mechanisms involved in biological control and growth promotion. indirect from the plant (Pathania et al., 2020).
The regulation of biotic and abiotic stresses by bacteria was also highlighted among the articles, where saline, water, heavy metal and thermal stress were studied. The control of salt stress was the second most discussed biostimulant effect, this fact is related to the constant growth of areas affected by salt, where the forecast is that 50% of arable areas globally will be affected. Damage to photosynthetic machinery, losses in plant development and losses in productivity are some of the harmful effects of salt (Abbas et al., 2019).
When subjected to saline stress, inoculated plants presented in the study demonstrate numerous mechanisms to overcome the problem such as the production of cytokines, accumulation of abscisic acid (ABA), production of antioxidants against ROS, such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR) and non-enzymatic antioxidants such as comotocopherols, ascorbate, cysteine and glutathione, all involved in the degradation of ROS (Shultana et al., 2022). Osmolytes are also key substances produced by PGP bacteria, such as proline, glycine and betaine, which are accumulated in plants with multifunctional roles such as protein maintenance, regulation of cytosolic acidity, reduction of lipid peroxidation and elimination of ROS, favoring cellular homeostasis (Abbas et al., 2019; Babar et al., 2021).
PGPs bacteria also increase plant photosynthesis, the content of photosynthetic pigments, stomatal conductance, regulate the rate of transpiration and the efficiency of photosystem II both under normal conditions and under stress, especially under water stress (Uarrota et al., 2022). The fact that PGPs bacteria can control stomatal opening and closing helps minimize water losses, mainly through the production of ABA that accumulates in response to water stress produced in the plant's chloroplasts and roots. This hormone is transferred to guard cells promoting stomatal closure (Gowtham et al., 2022).
Inoculation promotes greater supplies of nutrients such as NPK, which are essential for the biosynthesis of photosynthetic pigments, especially under stress conditions for the conservation of the photosynthetic system. This fact may be related to the higher quantum yield since photosystem II (PSII), non-regulatory constitutive non-photochemical quenching quantum yield ratio (PQ), chlorophyll fluorescence (qTQ) and variable chlorophyll fluorescence (qTV) are positively regulated (Khanghahi et al., 2020).
Gene regulation is also altered mainly with the identification of stress-responsive genes. High transcription levels of genes for coding antioxidant proteins (ZmGR1 and ZmAPX1) and genes involved in salt tolerance (ZmNHX1, ZmNHX2, ZmNHX3, ZmWRKY58 and ZmDREB2A) are reported (Li et al., 2020). These findings are part of accessing the complete mRNA transcriptome, present in a cell at any stage or under any environmental conditions. When studying gene expression in rapeseed inoculated with Stenotrophomonas rhizophila, through transcriptomic analysis, the recognition of spermidine, a growth regulator, formed under abiotic stress was verified (Alavi et al., 2013).
Growth promotion and salt stress control are the main applications of PGPs bacteria, with Bacillus and Pseudomonas being the most recurrent bacterial genera. The botanical families Fabaceae and Poaceae stand out in the bacteria/plant interaction, representing the highest percentages of studies in this area, with greater emphasis on crops such as Zea mays L. and Glycine max L.
Bacterial inoculation promotes beneficial effects on plant physiology, positively regulating photosynthetic parameters, improving stomatal conductance, increasing the production of proline and photosynthetic pigments, reducing lipid peroxidation, increasing nutritional and hormonal levels, producing antioxidant enzymes, antimicrobial substances, as well as an increase in the expression of genes related to plant adaptation to environmental stresses. These results elucidate the physiological modulation of the plant and direct future studies to specific physiological analyzes to facilitate the understanding of environmental responses regarding the plant-bacteria association, mainly to understand the symbiosis in the face of environmental stresses.
Supplementary Material
Supplementary material accompanies this paper.
Supplementary material
This material is available as part of the online article from https://doi.org/10.1590/1519-6984.287279
Acknowledgements
To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for granting the scholarship to Fernanda Viana Diniz. To the Fundação de Amparo à Pesquisa no Estado do Acre (FAPAC) for financing the project entitled “Bactérias endofíticas de cacau (Theobroma cacao L.) para promoção de crescimento vegetal e controle biológico de Moniliophthora perniciosa”.
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