Tolerance of upland rice cultivars to aluminum and acidic pH

Tolerância de cultivares de arroz de terras altas ao alumínio e pH ácido

ABSTRACT

Although the upland rice has been known by its moderate tolerance to aluminum, the presence of exchangeable aluminum in acidic soils may inhibit and compromise the adequate plant growth. However, there are few reports detailing modern cultivars used by Brazilian farmers with respect to their susceptibility to aluminum toxicity. This study aimed to characterize the cultivars currently used in the upland rice production with respect to their tolerance to aluminum and their growth under low pH conditions without aluminum. The treatments were arranged in a randomized block design, in a 2 x 9 factorial scheme: presence and absence of aluminum in the nutrient solution and nine upland rice cultivars (BRS Monarca, BRS Pepita, BRS Bonança, BRS Primavera, BRS Sertaneja, Maravilha, IAC 202, ANCambará and ANa7007), with four replicates. Based on the distribution of upland rice cultivars in quartiles, they were divided into two groups; aluminum-tolerant group: BRS Pepita, BRS Primavera and ANa7007; and aluminum-susceptible group: BRS Monarca, BRS Bonança, BRS Sertaneja, Maravilha, IAC 202 and ANCambará.

Key words:
Oryza sativa L.; aluminum susceptibility; aluminum resistance

RESUMO

Apesar de o arroz de terras altas ser reconhecido por sua moderada tolerância ao alumínio, a presença de alumínio trocável em solos ácidos pode inibir e comprometer o crescimento adequado das plantas; no entanto, poucos são os relatos descrevendo, de forma detalhada, os cultivares modernos utilizados pelos agricultores brasileiros quanto a sua susceptibilidade à toxicidade de alumínio. Objetivou-se neste estudo caracterizar os cultivares atualmente utilizados na produção de arroz de terras altas em relação à tolerância ao alumínio e ao seu crescimento sob cultivo em condição de baixo pH sem alumínio. Os tratamentos foram dispostos em um delineamento em blocos casualizados, em esquema fatorial 2 × 9: presença e ausência de alumínio na solução nutritiva e nove cultivares de arroz de terras altas (BRS Monarca, BRS Pepita, BRS Bonança, BRS Primavera, BRS Sertaneja, Maravilha, IAC 202, ANCambará e ANa7007), com quatro repetições. Com a distribuição dos cultivares de arroz de terras altas em quartis foi possível diferenciar os cultivares em dois grupos. Grupo tolerante ao Al³⁺: BRS Pepita, BRS Primavera e ANa7007; grupo suscetível ao Al³⁺: BRS Monarca, BRS Bonança BRS Sertaneja, Maravilha, IAC 202 e ANCambará.

Palavras-chave:
Oryza sativa L.; alumínio susceptibilidade; resistência à alumínio

Introduction

Upland rice is considered as a plant moderately tolerant to aluminum (Al³⁺) (Fageria, 1998) but its growth may be inhibited or reduced in soils with high contents of Al³⁺ (Mendonça et al., 2003; Freitas et al., 2006).

The roots of plants under stress by Al³⁺ have their growth interrupted and become stunted, breakable, with a few fine ramifications, increased rigidity and thickness of the cell wall and suffer alterations in the membrane proteins (Meriga et al., 2010; Motoda et al., 2010; Sun et al., 2010; Garzon et al., 2011; Guo et al., 2012). Consequently, the roots become inefficient in the uptake of water and nutrients, especially in deeper soil layers (Mendonça et al., 2003; Sun et al., 2010).

Modern upland rice cultivars are less tolerant to Al³⁺ in comparison to the traditional ones (Justino et al., 2006) due to the process of genetic improvement, through which the cultivars have lost this characteristic. In this context, there are few reports thoroughly describing the modern cultivars used by Brazilian farmers with respect to their susceptibility to Al³⁺.

There are only descriptions of the susceptibility of upland rice lines to Al³⁺ (Guimarães et al., 2006) and studies restricted to a small number of cultivars, which evaluate one tolerant and one non-tolerant cultivar to Al³⁺ (Mendonça et al., 2003; Justino et al., 2006). Therefore, this study aimed to characterize the cultivars currently used in the production of upland rice with respect to their tolerance to Al³⁺ and growth cultivated under low pH condition without aluminum.

Material and Methods

Two experiments were carried out in a greenhouse at the Department of Soils and Environmental Resources of the Faculty of Agronomic Sciences, UNESP, Botucatu, SP.

Experiment I: Upland rice tolerance to Al³⁺ toxicity in nutrient solution

The experimental design was in randomized blocks, in a 2 x 9 factorial scheme, with four replicates. The treatments consisted of the presence and absence of Al³⁺ in the nutrient solution and nine upland rice cultivars (Embrapa - BRS Monarca, BRS Pepita, BRS Bonança, BRS Primavera, BRS Sertaneja and Maravilha; Agronomic Institute of Campinas (IAC) - IAC 202; Agronorte - ANCambará and ANa7007). The evaluated cultivars were selected among the most used ones in upland rice-producing regions. Embrapa, Agronorte and IAC were contacted and provided this information and the seeds.

The experiment used the nutrient solution described by the study of Al³⁺ tolerance of rice plants developed by Furlani & Furlani (1988) and adapted by Zonta (2003), which was composed of 1.42 Ca, 1.51 K, 0.33 Mg, 0.95 N-NO₃, 0.41 N-NH₄, 0.01 P, 0.21 S, 0.21 Cl, 0.22 Fe, 0.009 Mn, 0.008 B, 0.00076 Zn and 0.00031 Cu mmol L^-1. The concentration and source of Al³⁺ were 1.48 mmol L^-1 and AlCl₃.6H₂O, respectively.

In order to obtain seedlings for the experiment, the rice seeds were treated with carboxin + thiram (400 mL per 100 kg of seeds) and then placed to germinate in germinators with controlled light (12 h) and temperature (25 ^oC).

After the period of seed germination, the seedlings were selected with respect to uniformity in form and size and transferred to plastic pots containing 4 L of nutrient solution, at half ionic strength. Polystyrene lids were used to fix the plants in the pots (6 plants pot^-1).

At 7 days after transplanting (DAT), the solution was substituted and nutrient solution without dilution was added, which remained under these conditions until 21 DAT. After this period, the treatments with Al³⁺ were applied and the plants were cultivated with the treatments until 42 DAT.

During the entire experimental period, the nutrient solution was aerated and the pH was daily monitored, maintained around 4.0 (± 0.1) and corrected using NaOH (0.1 mol L^-1) and HCl (0.1 mol L^-1). The nutrient solution was weekly renewed by adding the respective treatments and the losses through evapotranspiration were daily replenished with demineralized water. Heaters were used in the greenhouse in order to maintain the temperature at approximately 25 ^oC.

Plants were evaluated for root mean length and diameter (WinRhizo); root dry matter, shoot dry matter and the “S” index of susceptibility to Al³⁺, according to Fisher & Maurer (1978) adapted by Guimarães et al. (2006) for Al³⁺ stress, as shown in Eqs. 1 and 2:

where:

D - severity of the applied stress;

Yi and Ys - root lengths without and with stress, respectively; and,

Yms and Ymi - mean root lengths of the experiment, with and without stress, respectively.

For the selection, the cultivars were distributed in quartiles, delimited by the mean root length, without the stress of Al³⁺ toxicity, plus 75% of its standard deviation and the mean of its Al³⁺ toxicity susceptibility index, minus 25% of its standard deviation. Thus, the lower the IS, the less affected the plants are by the stress level induced by Al³⁺ toxicity.

The data of the other variables were subjected to analysis of variance by F test and the means were compared by the Scott-Knott test, for cultivars, and F test for the comparison between the presence and absence of Al³⁺ treatments, both at 0.05 probability level.

Experiment II: Upland rice cultivation in aluminic soil

The experimental design was in randomized blocks, with four replicates, and the treatments were the same nine upland rice cultivars used in Experiment I. However, they were cultivated in pots containing aluminic soil (m% > 50%) and evaluated for the number of panicles per plant, grain production, shoot dry matter and harvest index of the cultivars under stress by Al³⁺. The harvest index was determined through the relationship of grain production/shoot dry matter production.

The soil used in the experiment was of low natural fertility and aluminic, classified as Dark Red Latosol, with medium sandy texture, which showed the following chemical characteristics: 7 mg dm^-3 of P-resin; 15 g dm^-3 of organic matter; 4.1 of pH in CaCl₂; 0.7, 5, 3, 69, 11 and 78 mmol_c dm^-3 of K, Ca, Mg, H + Al, Al³⁺ and CEC, respectively; and 55.8% of saturation by Al³⁺.

The data were subjected to analysis of variance and the means were compared by the Scott-Knott test at 0.05 probability level.

Results and Discussion

The cultivars were divided into two groups: the first one was composed of BRS Pepita, BRS Primavera and ANa7007, whose Al³⁺ susceptibility index of the root growth was lower than 0.93, being considered as tolerant to Al³⁺, while the second group was composed of the cultivars BRS Monarca, BRS Bonança, BRS Sertaneja, Maravilha, IAC 202 and ANCambará, which obtained Al³⁺ susceptibility index higher than 0.93, thus being considered as susceptible to Al³⁺ (Figure 1).

Figure 1
Distribution of the cultivars in quartiles delimited by the root length in 0 mg dm^-3 of aluminum and by the susceptibility index of root growth to aluminum toxicity, at the points determined by the mean root length (without Al³⁺) + 75% of its standard deviation and by the mean root susceptibility index to aluminum - 25% of its standard deviation

The cultivars BRS Monarca, BRS Bonança and ANCambará stand out for their higher root growth when grown in the absence of Al³⁺, i.e., only under the condition of high acidity (pH 4.0). It is worth remembering that the lower the Al³⁺ susceptibility index, the less affected the cultivar is by the deleterious effects of the Al³⁺.

It is interesting to note that the division by quartiles separated only three cultivars as tolerant to Al³⁺, according to the adopted criteria. Thus, although upland rice is considered as a plant moderately tolerant to Al³⁺ (Fageria, 1998), its growth can be influenced by Al³⁺, confirming the results reported by Ferreira et al. (1995), Mendonça et al. (2003) and Freitas et al. (2006).

The distribution of the cultivars in quartiles (root growth) was used to separate them with respect to the tolerance to Al³⁺; however, from this point on, the cultivars will be evaluated considering their efficiency under stress by Al³⁺, as well as in cultivation in the absence of Al³⁺, since they were cultivated at pH 4.0, which is close to the pH at which the upland rice crop is cultivated especially in recently deforested areas.

The cultivar BRS Monarca showed higher shoot and root dry matter production when cultivated in the presence and absence of Al³⁺ (Table 1). On the other hand, comparing the cultivation in the presence and absence of Al³⁺, the shoot dry matter production of the cultivars BRS Monarca, Maravilha and ANa7007 were lower in the presence of Al³⁺.

Table 1
Shoot and root dry matter production of upland rice cultivars grown in the presence (+Al³⁺) and absence (-Al³⁺) of aluminum

• Means followed by different letters, uppercase in rows and lowercase in columns, differ statistically at 0.05 probability level by Scott-Knott tests, respectively

The cultivars BRS Pepita and ANa7007 were classified as tolerant to Al³⁺ according to the method of separation by quartiles (Figure 1); hence, it can be noted that, in comparison to the other cultivars, these two produce lower amount of shoot dry matter. Thus, it is possible that this variable is little influenced by Al³⁺ toxicity caused to the roots. Therefore, this variable is probably not indicated for the classification of cultivars regarding their tolerance to Al³⁺.

The cultivars BRS Pepita, Maravilha and ANa7007 obtained lower root dry matter production when cultivated in the presence and absence of Al³⁺; however, among the cultivars, only BRS Pepita was not different in the comparison of cultivation in the presence and absence of Al³⁺.

It is known that root dry matter production is negatively influenced by the action of Al³⁺ (Roy & Bhadra, 2014). Despite the lower root dry matter production in the presence of Al³⁺ (Table 1), the cultivars BRS Pepita and ANa7007 were considered as tolerant through the separation in quartiles (Figure 1). Thus, the methodology of separation into quartiles is important to distinguish the cultivars and it is basically a relationship between root length in the presence and in the absence of Al³⁺. Therefore, both cultivars showed lower difference between the root growth in the presence and absence of Al³⁺ in comparison to the others.

It is also necessary to consider that, before root dry matter shows a decrease caused by Al³⁺ toxicity, this phytotoxic element acts first in root elongation and, consequently, leads to lower root length (Sun et al., 2010; Roy & Bhadra, 2014).

The cultivars BRS Monarca, BRS Bonança and ANCambará showed greater root length when grown in the absence of Al³⁺ in comparison to the others (Table 2). This behavior can contribute to explaining the classification of the cultivar BRS Monarca as susceptible to Al³⁺ (Figure 1), since there was great amplitude between the root growth in the absence and presence of Al³⁺, evidencing the damaging action of Al³⁺.

Table 2
Root length and diameter of upland rice cultivars grown in the presence (+Al³⁺) and absence (-Al³⁺) of aluminum

• Means followed by different letters, uppercase in rows and lowercase in columns, differ statistically at 0.05 probability level by Scott-Knott tests, respectively

On the other hand, it is observed that the cultivar ANa7007 in the presence of Al³⁺, despite showing lower shoot and root dry matter production (Table 1), has the greatest root length among all cultivars when grown under stress by Al³⁺ (Table 2), confirming its selection as tolerant to Al³⁺ (Figure 1).

The cultivar ANa7007 showed the lowest root diameter in both types of cultivation (absence and presence of Al³⁺) (Table 2); this behavior can contribute to explaining the low root dry matter production of this cultivar (Table 1).

The root diameter referring to the cultivation in the absence of Al³⁺ can be considered as a reference for comparison (Table 2) due to the increment in root diameter caused by Al³⁺ toxicity (Motoda et al., 2010). Hence, comparing the cultivars in the presence and absence of Al³⁺, the effect of root thickening favored by the toxicity occurred for almost all the cultivars, except for ANa7007.

The cultivar BRS Monarca stands out for the increment of 0.107 mm in mean root diameter, in the comparison of cultivated in the presence and absence of Al³⁺, and it was the highest value observed among the nine tested cultivars (Table 2). Therefore, this variable can also support the selection of this cultivar as susceptible to Al³⁺.

Given the presented results and in general, the cultivars BRS Monarca, BRS Bonança, BRS Primavera, BRS Sertaneja, IAC 202 and ANCambará obtained adequate growth without the presence of Al³⁺ and at acidic pH (4.0); thus, these cultivars are interesting for cultivation in soils with acidic pH, but without high content of Al³⁺, while the cultivars BRS Pepita and Maravilha obtained lower growth when cultivated in the presence of Al³⁺.

Even in the presence of Al³⁺, the cultivar BRS Monarca showed good dry matter production (Table 1); in spite of that, it showed small root growth when cultivated under these conditions (Table 2), being strongly affected by this phytotoxic ion. In contrast, the cultivar ANa7007 stood out as tolerant to Al³⁺ (Figure 1) due to the high root growth obtained under stress by Al³⁺ (Table 2); however, it showed the lowest shoot and root dry matter production among the evaluated cultivars (Table 1). Therefore, it is suggested to study methodologies for the selection of cultivars tolerant and susceptible to Al³⁺ in order to increase the efficiency of the test and obtain greater understanding about the reflex of the variables root dry matter and root length on grain production, since not always a plant is able to produce large amount of root dry matter or the shoots are able to convert this produced dry matter into grains; ultimately, this is the objective of the rural producer.

To reinforce the results of the Experiment I (nutrient solution), a second experiment was conducted with the same cultivars; however, they were grown in pots with aluminic soil (Table 3).

Table 3
Number of panicles plant^-1, grain production, shoot dry matter and harvest index of upland rice cultivars grown in aluminic soil

• Means followed by different letters for each parameter differ by the Scott-Knott test at 0.05 probability level

The cultivars BRS Primavera and ANa7007 showed higher grain production and also low shoot dry matter production, demonstrating good harvest index. These results reinforce the definition of the cultivars BRS Primavera and ANa7007 as tolerant to Al³⁺ (Figure 1), which showed interesting agronomic characteristics for high yield (Table 3).

As to the cultivars BRS Sertaneja and Maravilha, selected as susceptible to Al³⁺ based on the experiment in nutrient solution (Figure 1), despite obtaining the highest shoot dry matter production among the tested cultivars (Table 3), they showed low grain production and, consequently, the worst harvest index among the cultivars. Therefore, their definition as susceptible to Al³⁺ is reinforced. These results were similar to those reported by Mendonça et al. (2003) and Justino et al. (2006), who also observed the susceptibility of the cultivar Maravilha to Al³⁺.

These results demonstrate that shoot dry matter production may not be efficient in the selection of the cultivars, because the cultivar BRS Sertaneja showed higher shoot dry matter production, but its grain production was lower compared with the cultivars that produced less shoot dry matter (Table 3).

Lastly, studies like these are initially important since they are basic experiments, i.e., it is the first study to be conducted aiming to obtain possible characteristics of tolerance to Al³⁺ in cultivars. However, it is important to evaluate the studied cultivars in field experiments and in different regions, because it is the only way to permanently differentiate the cultivars with respect to their tolerance to Al³⁺.

Conclusions

1. With the distribution of the upland rice cultivars in quartiles, it was possible to differentiate them in two groups. Al³⁺ tolerant group: BRS Pepita, BRS Primavera and ANa7007; Al³⁺ susceptible group: BRS Monarca, BRS Bonança BRS Sertaneja, Maravilha, IAC 202 and ANCambará.

2. The cultivars BRS Primavera and ANa7007 show higher grain production when cultivated in aluminic soil.

3. The cultivars BRS Monarca, BRS Bonança, BRS Primavera, BRS Sertaneja, IAC 202 and ANCambará have adequate growth when cultivated in nutrient solution with acidic pH (4.0) and in the absence of Al³⁺.

Acknowledgments

To the São Paulo Research Foundation (FAPESP), for the financial support granted through the doctorate scholarship to the first author (grant #2011/09283-0) and the project of regular support to the research (grant # 2011/22182-8).

To the National Council for Scientific and Technological Development (CNPq) for providing a research grant to the second author.

To the Brazilian Agricultural Research Corporation (EMBRAPA), AGRONORTE and the APTA Regional/SAASP - Centro Oeste, for providing the seeds of the evaluated upland rice cultivars.

Literature Cited

• Fageria, N. K. Otimização da eficiência nutricional na produção das culturas. Revista Brasileira de Engenharia Agrícola e Ambiental, v.2, p.6-16, 1998. http://dx.doi.org/10.1590/1807-1929/agriambi.v02n01p6-16
  » http://dx.doi.org/10.1590/1807-1929/agriambi.v02n01p6-16
• Ferreira, R. P.; Cruz, C. D.; Sediyama, C. S.; Fageria, N. K. Identificação de cultivares de arroz tolerantes à toxidez de alumínio por técnica multivariada. Pesquisa Agropecuária Brasileira, v.30, p.789-795, 1995.
• Fisher, R. A.; Maurer, R. Drought resistance in spring wheat cultivars. I. Grain yield responses. Australian Journal of Agricultural Research, v.29, p.897-912, 1978. http://dx.doi.org/10.1071/AR9780897
  » http://dx.doi.org/10.1071/AR9780897
• Freitas, F. A.; Kopp, M. M.; Sousa, R. O.; Zimmer, P. D.; Carvalho, F. I. F.; Oliveira, A. C. Absorção de P, Mg, Ca e K e tolerância de genótipos de arroz submetidos a estresse por alumínio em sistemas hidropônicos. Ciência Rural, v.36, p.72-79, 2006. http://dx.doi.org/10.1590/S0103-84782006000100011
  » http://dx.doi.org/10.1590/S0103-84782006000100011
• Furlani, P. R.; Furlani, A. M. Composição de pH de solução nutritiva para estudos fisiológicos e seleção de plantas em condições nutricionais adversas. Campinas: Instituto Agronômico, 1988. 34p. Boletim Técnico, 121
• Garzon, T.; Gunse, B.; Moreno, A. R.; Tomos, A. D.; Barcelo, J.; Poschenrieder, C. Aluminium-induced alteration of ion homeostasis in root tip vacuoles of two maize varieties differing in Al tolerance. Plant Science, v.180, p.709-715, 2011. http://dx.doi.org/10.1016/j.plantsci.2011.01.022
  » http://dx.doi.org/10.1016/j.plantsci.2011.01.022
• Guimarães, C. M.; Neves, P. C. F.; Stone, L. F.; Zimmermann, F. J. P. Resistência do arroz de terras altas ao alumínio. Revista Brasileira de Engenharia Agrícola e Ambiental, v.10, p.855-860, 2006. http://dx.doi.org/10.1590/S1415-43662006000400011
  » http://dx.doi.org/10.1590/S1415-43662006000400011
• Guo, T. R.; Yao, P. C.; Zhang, Z. D.; Wang, J. J.; Wang, M. Involvement of antioxidative defense system in rice growing seedlings exposed to aluminum toxicity and phosphorus deficiency. Rice Science, v.19, p.207-2012, 2012. http://dx.doi.org/10.1016/S1672-6308(12)60042-0
  » http://dx.doi.org/10.1016/S1672-6308(12)60042-0
• Justino, G. C.; Cambraia, J.; Oliva, M. A.; Oliveira, J. A. Absorção e redução de nitrato em duas cultivares de arroz na presença de alumínio. Pesquisa Agropecuária Brasileira, v.41, p.1285-1290, 2006. http://dx.doi.org/10.1590/S0100-204X2006000800011
  » http://dx.doi.org/10.1590/S0100-204X2006000800011
• Mendonça, R. J.; Cambraia, J.; Oliveira, J. A.; Oliva, M. A. Efeito do alumínio na absorção e na utilização de macronutrientes em duas cultivares de arroz. Pesquisa Agropecuária Brasileira, v.38, p.843-846, 2003. http://dx.doi.org/10.1590/S0100-204X2003000700008
  » http://dx.doi.org/10.1590/S0100-204X2003000700008
• Meriga, B.; Attitalla, I. H.; Ramgopal, M.; Ediga, A.; Kavikishor, P. B. Differential tolerance to aluminum toxicity in rice cultivars: Involvement of antioxidative enzymes and possible role of aluminum resistant locus. Academic Journal of Plant Sciences, v.3, p.53-63, 2010.
• Motoda, H.; Kano, Y.; Hiragami, F.; Kawamura, K.; Matsumoto, H. Morphological changes in the apex of pea roots during and after recovery from aluminum treatment. Plant Soil, v.333, p.49-58, 2010. http://dx.doi.org/10.1007/s11104-010-0318-1
  » http://dx.doi.org/10.1007/s11104-010-0318-1
• Roy, B.; Bhadra, S. Effects of toxic levels of aluminium on seedling parameters of rice under hydroponic culture. Rice Science, v.21, p.217-223, 2014. http://dx.doi.org/10.1016/S1672-6308(13)60182-1
  » http://dx.doi.org/10.1016/S1672-6308(13)60182-1
• Sun, P.; Tian, Q. Y.; Chen, J.; Zhang, W. H. Aluminum-induced inhibition of root elongation in Arabidopsis is mediated by Ethylene and Auxin. Journal of Experimental Botany, v.61, p.346-356, 2010. http://dx.doi.org/10.1093/jxb/erp306
  » http://dx.doi.org/10.1093/jxb/erp306
• Zonta, E. Estudos da tolerância ao alumínio em arroz de sequeiro e seus efeitos sobre a interface solo-planta. Rio de Janeiro: UFRJ, 2003. 139p. Tese Pós-Doutorado

Publication Dates

• Publication in this collection
  Oct 2016

History

• Received
  25 Oct 2015
• Accepted
  01 Sept 2016