Agrarian Academic Journal
doi: 10.32406/v8n1/2025/1-12/agrariacad
Physiological and biochemical characterization of contrasting cowpea genotypes for drought tolerance. Caracterização fisiológica e bioquímica de genótipos de feijão-caupi contrastantes para tolerância à seca.
Eveline Nogueira Lima
1, Cândida Hermínia Campos de Magalhães2, Rosilene Oliveira Mesquita3, Angela Maria dos Santos Pesssoa4, Ingrid Bernardo de Lima Coutinho5
1- Engenheira Agrônoma – Universidade Federal do Ceará – UFC, Campus Pici – Fortaleza/CE. E-mail: evelinenlima@gmail.com
2- Professora Associada – Universidade Federal do Ceará – UFC, Campus Pici – Fortaleza/CE. E-mail: candida@ufc.br
3- Professora Associada – Universidade Federal do Ceará – UFC, Campus Pici – Fortaleza/CE. E-mail: rosilenemesquita@gmail.com
4- Departamento de Fitotecnia, Universidade Federal Rural do Semiárido – UFERSA, Mossoró/RN. E-mail: angelapessoapb@gmail.com, angela.pessoa@ufersa.edu.br
5- Engenheira Agrônoma – Universidade Federal do Ceará – UFC, Campus Pici – Fortaleza/CE. E-mail: ibernardodelima@gmail.com
Abstract
The objective of this study was to understand the physiological and biochemical mechanisms of drought tolerance in contrasting cowpea genotypes. The experiment was carried out in a greenhouse at the Federal University of Ceará, State of Ceará, Brazil. A stress-tolerant (Pingo de Ouro 1.2) and sensitive (Santo Inácio) cowpea genotype was grown under total irrigation (control), moderate water deficit, severe water deficit and re-irrigation after severe water deficit to study its mechanisms of water drought tolerance. The experimental design was completely randomized in a 4×2 factorial scheme, with five replications. The factors corresponded to irrigation regimes and genotypes. The results indicated that the main mechanisms of drought tolerance in cowpea include greater leaf water potential and electron transport rate under conditions of severe water deficit. In addition, maintaining the chlorophyll content, increasing the content of carbohydrates and amino acids in the leaves for osmotic adjustment, less damage to the cell membrane and greater recovery capacity after rehydration were observed as the main mechanisms. Therefore, Pingo de Ouro 1.2 was more tolerant of water stress.
Keywords: Osmotic adjustment. Oxidative stress. Vigna unguiculata. Water stress.
Resumo
O objetivo deste estudo foi compreender os mecanismos fisiológicos e bioquímicos da tolerância à seca em genótipos contrastantes de feijão-caupi. O experimento foi conduzido em casa de vegetação na Universidade Federal do Ceará, Estado do Ceará, Brasil. Um genótipo de feijão-caupi tolerante ao estresse (Pingo de Ouro 1.2) e sensível (Santo Inácio) foi cultivado sob irrigação total (controle), déficit hídrico moderado, déficit hídrico grave e re-irrigação após déficit hídrico grave para estudar seus mecanismos de tolerância à seca. O delineamento experimental foi inteiramente casualizado em esquema fatorial 4×2, com cinco repetições. Os fatores corresponderam aos regimes de irrigação e genótipos. Os resultados indicaram que os principais mecanismos de tolerância à seca no feijão-caupi incluem maior potencial hídrico foliar e taxa de transporte de elétrons em condições de déficit hídrico severo. Além disso, a manutenção do teor de clorofila, aumento do teor de carboidratos e aminoácidos nas folhas para ajuste osmótico, menor dano à membrana celular e maior capacidade de recuperação após a reidratação foram observados como os principais mecanismos. Portanto, o Pingo de Ouro 1.2 foi mais tolerante ao estresse hídrico.
Palavras-chave: Ajuste osmótico. Estresse oxidativo. Vigna unguiculata. Estresse hídrico.
Introduction
Cowpea [Vigna unguiculata (L.) Walp.] is cultivated mainly in the North and Northeast of Brazil (NASCIMENTO et al., 2011). Thes crop is of great importance especially for the poor people in these regions, since cowpea grains are very accepted, have high nutritional value, and represent one of the main food sources in the diet (SILVA et al., 2010).
Besides being used for human consumption, cowpea can be used as animal feed, forage, green manure, and soil mulch (CARDOSO et al., 2017). Thus, the use of more productive varieties in the family farming system is of great economic importance to rural farmers (SANTOS et al., 2009a). However, water deficit condition in the Northeastern region is one of the main factors reducing cowpea productivity (MENDES et al., 2007).
The water deficit affects many crops reducing their productivity by influencing almost all aspects related to plant development (DAMATTA, 2007). Damages vary according to stress duration, intensity, frequency, and time of occurrence, as well as according to plant genotype. Frequency and intensity of water deficit are the most important factors limiting the world agricultural production (SANTOS; CARLESSO, 1998).
Although considered tolerant to low water availability conditions, when compared to other crops, such as common bean (Phaseolus vulgaris), studies have shown that cowpea was moderately sensitive to water stress (BELKO et al., 2012). According to Lima et al. (2006), the water requirement of cowpea plants varies with the development stage, increasing from a minimum value on germination to a maximum value on flowering and pod formation, then decreasing at the beginning of maturation.
Considering the importance of cowpea for the North and Northeast of Brazil, it is essential to evaluate the performance of cultivars developed for dryland cultivation, in view of the imposed water limitations in the different crop growth stages. According to Sousa et al. (2009), water stress decreases the productivity in common bean and is more severe when it occurs in the flowering and fruiting phases. In cowpea, many adaptive mechanisms to drought have been described by several authors (SANTOS et al., 2010; NASCIMENTO et al., 2011; BASTOS et al., 2012; RIVAS et al., 2016) showing how this crop is resistant to drought and heat.
In cowpea breeding programs, the selection of genotypes with drought tolerance characteristics is important to ensure production, mainly in the semiarid regions, where rainfall is poorly distributed and, in recent years, prolonged periods of drought have been observed. Thus, this study aimed to understand physiological and biochemical mechanisms for drought tolerance in contrasting cowpea genotypes.
Material and methods
The experiment was carried out under greenhouse conditions at Federal University of Ceará, Brazil, where the temperature is 35±5 ºC and relative humidity is 70±20%. Two cowpea (V. unguiculata) genotypes, a tolerant (Pingo de Ouro 1,2) and other sensitive (Santo Inácio) to water deficit (NASCIMENTO et al., 2011; RIVAS et al., 2016), were cultivated using seeds provided by Embrapa Mid-North (Teresina, Piauí, Brazil) and Germplasm Bank from Federal University of Ceará, respectively. Three seeds of each genotype were sown in pots with 11 L capacity filled with a substrate composed of sand, vermicompost and vermiculite (at 6:3:1 ratio by volume). Irrigation was performed daily and 10 days after sowing (DAS) a thinning was carried out maintaining one seedling per pot.
When reached the pre-flowering stage (V4), plants were subjected to four irrigation regimes: (1) full irrigation (control); (2) moderate water deficit [–1.0±0.1 MPa leaf predawn water potential (Ypd)]; (3) severe water deficit (-1.5±0.1 MPa Ypd); and (4) plant rehydration condition. In the fourth treatment, after being subjected to severe deficit, the plants were re-irrigated and evaluated four days after rehydration, to evaluate the recovery response to drought.
Data were collected when plants reached the desired water potential through measurements with a Scholander pressure pump (SCHOLANDER et al., 1965).
Cowpea leaves and roots were collected and stored in aluminized paper envelopes, frozen in liquid nitrogen, and stored at –80 °C for further analysis. They were dried in a lyophilizer and then macerated to a fine powder which was stored.
The experimental design was completely randomized in a 4×2 factorial scheme, with five replicates. Factors corresponded to the four irrigation regimes and the two genotypes. Data were subjected to two-way analysis of variance (p <0.05) and means were grouped by the Tukey test (p<0.05). Statistical analyses were performed using the Sisvar software (Ferreira, 2011), and graphs were designed using the SigmaPlot 11.0 (Systat Software Inc, 2008).
Characterization of physiological and biochemical responses
Ten days after the water deficit imposition, leaf water potential (Ψw) was evaluated in fully expanded leaves of the fourth or fifth trifolium from the apex between 05:30 and 06:30 a.m. using a Scholander pressure pump (SCHOLANDER et al., 1965).
Chlorophyll a fluorescence
Chlorophyll a fluorescence was measured using an IRGA-coupled fluorometer (IRGA, LI-6400XT, LI-COR Biosciences Inc., Lincoln, Nebraska, USA). The fluorescence induction variables obtained were initial fluorescence (Fo); maximum fluorescence (Fm); variable fluorescence (Fv), obtained by Fo – Fm; and maximum quantum yield of photosystem II (PSII) (Fv/Fm) (GENTY et al., 1989). Also, electron transport rate (ETR) and actual quantum yield of PSII photochemistry (φPSII) were obtained (GENTY et al., 1989).
Photosynthetic pigments
Chlorophyll a (Chl a), chlorophyll b (Chl b), total chlorophyll (Chl a+b), and carotenoid contents were determined by the method described by Wellburn (1994), based on the following equations:
Chl a = (12.47 × A665) – (3.62 × A649) (Equation 1)
Chl b = (25.06 × A649) – (6.5 × A665) (Equation 2)
Chl a+b = (7.15 × A665) + (18.71 × A649) (Equation 3)
Carotenoid = (1000 × A480 – 1.29 × Chl a – 53.78 × Chl b) / 220 (Equation 4)
Where A represents the absorbance at the respective wavelength. Results were expressed as µg mL-1.
Lipid peroxidation
Lipid peroxidation was determined by quantifying malondialdehyde (MDA) levels produced under thiobarbituric acid (TBA) reaction, as previously described by Heath and Packer (1968). MDA contents were expressed as ηmol g-1 DW.
Organic solutes
Soluble carbohydrate content was obtained according to Dubois et al. (1956) and the soluble amino acid content was determined according to Yemm et al. (1955).
Results
Water potential
Under fully irrigated conditions, both Santo Inácio (sensitive) and Pingo de Ouro 1.2 (tolerant) cowpea genotypes showed similar predawn leaf water potential (Ψpd), -0.04 MPa. When the water supply was withdrawn, Santo Inácio required ten days to reach Ψpd from -1.0 to -1.5 Mpa, while Pingo de Ouro 1.2 required about 12 days to reach the same Ψpd levels (Figure 1). Such a result demonstrates greater water saving in Pingo de Ouro 1.2.
Figure 1 – Leaf water potential (MPa) in cowpea genotypes under water deficit conditions. Pingo de Ouro 1.2: tolerant to water deficit; Santo Inácio: sensitive to water deficit.
Chlorophyll a fluorescence
Regarding the chlorophyll a fluorescence, our results indicate that the maximum quantum yield of PSII (Fv/Fm) was similar in both genotypes evaluated in this experiment (Figure 2A). The only difference was detected under re-irrigated conditions, when Santo Inácio showed superior Fv/Fm values.
On the other hand, Pingo de Ouro 1.2 showed lower φPSII than Santo Inácio only under fully irrigated conditions (Figure 2B), but not differing in the water stress treatments.
Figure 2 – Chlorophyll a fluorescence: a) maximum quantum yield of PSII (Fv/Fm) and b) actual quantum yield of PSII photochemistry (φ PSII) in cowpea genotypes under water deficit conditions. Pingo de Ouro 1.2: tolerant to water deficit; Santo Inácio: sensitive to water deficit. Data are mean standard error (n = 5). Different uppercase letters indicate a significant difference between genotypes under the same irrigation regime, while different lowercase letters indicate a significant difference among irrigation regimes (Tukey test, p <0.05).
Under water stress conditions, ETR reduced proportionally with the stress level in both genotypes (Figure 3). Such results indicate that both genotypes were sensitive to water deficit.
Figure 3 – Electron transport rate (ETR) in cowpea genotypes under water deficit conditions. Pingo de Ouro 1.2: tolerant to water deficit; Santo Inácio: sensitive to water deficit. Data are mean standard error (n = 5). Different uppercase letters indicate a significant difference between means of the same treatment in different genotypes, and lowercase letters indicate a significant difference between means within the same genotype (Tukey test, p <0.05).
Photosynthetic pigments
Under severe water deficit conditions, the tolerant cultivar presented lower Chl a content than the sensitive one, not differing statistically from the other treatments. The sensitive genotype reduced Chl a under moderate water deficit but had the same contents under the severe and re-irrigated treatments. In turn, the tolerant genotype remained the same Chl a content under the control, moderate, and severe treatments, but increased under the re-irrigated treatment (Figure 4A). The tolerant genotype had higher Chl b contents under the control, moderate and re-irrigated treatments than the sensitive genotype, but lower under severe water deficit (Figure 4B). Chl a+b was different between genotypes only under the re-irrigated treatment (Figure 4C). The tolerant genotype reduced Chl a+b only under severe water deficit, while the sensitive genotype remained unchanged (Figure 4C). Regarding the carotenoid content, no difference was observed between genotypes and treatments (Figure 4D).
Figure 4 – Chlorophyll a (a), chlorophyll b (b), chlorophyll a+b (c) and carotenoid (d) contents in cowpea genotypes under water deficit conditions. Pingo de Ouro 1.2: tolerant to water deficit; Santo Inácio: sensitive to water deficit. Data are mean standard error (n = 5). Different uppercase letters indicate a significant difference between means of the same treatment in different genotypes, and lowercase letters indicate a significant difference between means within the same genotype (Tukey test, p <0.05).
Lipid peroxidation
Cell membrane damages were assessed by quantifying the malondialdehyde (MDA) levels in the leaves. An increased MDA content in the tolerant genotype was observed under moderate water deficit as compared to the severe and re-irrigated groups, not differing from the control. The sensitive genotype showed similar behavior to the tolerant one in almost all irrigation regimes. The tolerant genotype presented lower MDA content under re-irrigated treatment than under the control. MDA content in the sensitive genotype did not differ among the irrigation regimes, but increased under moderate stress, although not significantly different (Figure 5).
Figure 5 – Malondialdehyde (MDA) levels in leaves of cowpea genotypes under water deficit conditions. Pingo de Ouro 1.2: tolerant to water deficit; Santo Inácio: sensitive to water deficit. Data are mean standard error (n = 5). Different uppercase letters indicate a significant difference between means of the same treatment in different genotypes, and lowercase letters indicate a significant difference between means within the same genotype (Tukey test, p <0.05).
Soluble carbohydrate and amino acid contents
Soluble n-amino acids increased in leaves of both genotypes under water deficit. However, this solute increase in Pingo de Ouro 1.2 was higher than in Santo Inácio. A 70% increase was observed under severe water deficit as compared to control (Figure 6A). As in the leaves, the soluble n-amino acid content also increased in the roots under water deficit conditions in both genotypes. However, the tolerant genotype had 28% higher n-amino acid content in the roots than the sensitive one under the control treatment (Figure 6B).
Soluble carbohydrate content in Pingo de Ouro 1.2 leaves reduced under moderate and severe water deficit, as well as under re-irrigated treatment as compared to control. In Santo Inácio, the carbohydrate content remained constant (Figure 6C). In roots, the content did not differ in the tolerant genotype, but the sensitive one presented higher carbohydrate content under moderate and re-irrigated treatment than control. Santo Inácio had 20% higher carbohydrate content in the roots under re-irrigated treatment relative to control.
Discussion
Leaf water potential results (Figure 1) showed that Pingo de Ouro 1.2 was more efficient in water use than Santo Inácio. Pingo de Ouro 1.2 has some mechanisms that allow it to save water since it took about 12 days to reach the same Ψpd levels as Santo Inácio. Indeed, cowpea cultivars present different responses under abiotic stress due to their different physiological, biochemical, and anatomical characteristics (SANTOS et al., 2009b).
Rivas et al. (2016) also observed that these two cultivars respond differently to water stress, which suggests that there is a drought tolerance mechanism to maintain the stem water status. Nascimento et al. (2011) classified Pingo de Ouro 1.2 as a drought-tolerant cultivar able to maintain production under low water availability.
A decrease in Fv/Fm indicates a decline in the photochemical efficiency of PSII and a disturbance or damage in the photosynthetic apparatus (PERCIVAL et al., 2003). Such a variable is used to detect disturbances in the photosynthetic system caused by stress. According to Bolhàr-Nordenkampf (1989), when plants are not under stress conditions, Fv/Fm ranges from 0.75 to 0.85. In this study, cowpea plants under moderate and severe water deficit conditions showed Fv/Fm values within that range, which indicates no damages to the PSII, but the electron transport rate (ETR) was also significantly reduced due to the stress conditions.
Figure 6 – Soluble carbohydrates and n-amino acid contents in leaves and roots of cowpea genotypes under water deficit conditions. Pingo de Ouro 1.2: tolerant to water deficit; Santo Inácio: sensitive to water deficit. Data are mean standard error (n = 5). Different uppercase letters indicate a significant difference between means of the same treatment in different genotypes, and lowercase letters indicate a significant difference between means within the same genotype (Tukey test, p <0.05).
Pingo de Ouro 1.2, the tolerant cultivar, showed the same Chl content under water deficit and full irrigated conditions. This response is an important feature since it increases the plant efficiency in absorbing solar radiation and, consequently, improves its photosynthetic rate.
On the other hand, under severe stress, Chl content reduced as a response to increased formation and action of reactive oxygen species (ROS) that degrade the Chl molecules and chloroplast membranes (CARVALHO et al., 2003). ROS destroys the thylakoid membranes, releasing the content within the chloroplasts, including Chl b, to the cytosol (MARCONDES; GARCIA, 2009). Nascimento et al. (2011) also reported the Chl content decrease in cowpea genotypes under water deficit conditions.
Studying the lipid peroxidation is important since damages on leaf cell membranes indicate stress signals (FAROOQ et al., 2009). Thus, high MDA and hydrogen peroxide (H2O2) levels in the leaves indicate oxidative stress in plants. In the present study, the tolerant cowpea genotype presented lower contents of these compounds under water deficit conditions and re-irrigated treatment than the sensitive one, indicating a higher capacity to recover after water stress. Such increased MDA content under water deficit and recovery capacity after re-irrigation was also observed by Alam et al. (2010) in soybean. In common bean, susceptible genotypes showed high MDA and hydrogen peroxide (H2O2) contents in the leaves under water stress, which was not observed in tolerant genotypes (ROSALES et al., 2012).
Under stress conditions, plants increase peroxidase activity and it may be the first enzyme to have altered activity, regardless of substrate used or stress imposed (SANTOS et al., 2010). Variation in peroxidase activity may be an adaptation of plant tissue to stress conditions (HARTER et al., 2014).
Carbohydrate and soluble amino acid contents increased under water stress as a mechanism for osmotic adjustment. Under stress conditions, starch is degraded by amylase producing reducing soluble sugars (KELLER et al., 1993). Moreover, in most plants, sucrose is the main sugar exported from source (leaves) to sink regions such as stem, vegetative buds, roots, and reproductive organs, where sucrose will be used for growth and storage. Thus, sucrose may also be hydrolyzed producing hexoses for the osmotic adjustment (SANTOS et al., 2010). Similarly, increased protease activity due to water stress contributes to degrading proteins into amino acids, which may also contribute to osmotic adjustment (KERBAUY, 2004).
Pingo de Ouro 1.2 (tolerant) took longer to reach the same Ψpd levels, indicating that it can save more water than Santo Inácio. Therefore, Pingo de Ouro 1.2 showed mechanisms to maintaining water potential and higher electron transport rate under water stress conditions. In addition, this tolerant genotype maintained Chl levels, increased N-amino acids, and decreased MDA contents as mechanisms to tolerate water stress and maintaining growth.
Our results showed Pingo de Ouro 1.2 has drought tolerance mechanisms not observed in Santo Inácio, confirming these genotypes are tolerant and susceptible cultivars to water stress, respectively.
Conclusion
Pingo de Ouro 1.2 was more tolerant to water stress for maintaining the Chl content, decreasing MDA, and accumulating amino acids in the leaves and roots. This variety resists severe water stress by accumulating amino acids in the leaves and reducing MDA when rehydrated, in addition to taking longer to reach the same Ψpd levels as Santo Inácio.
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Received on April 30, 2024
Returned for adjustments on January 29, 2025
Received with adjustments on January 31, 2025
Accepted on February 11, 2025
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