ABSTRACT
Graywater is an alternative method to increase the water supply for agricultural production in semi-arid regions. The objective of this study was to evaluate the effects of different irrigation depths of graywater on the gas exchanges and phytomass of millet plants with and without organic fertilization. The research was conducted under greenhouse conditions in Serra Talhada municipality in semiarid region of Brazil, in a randomized complete block design with a factorial (4 × 2 + 1) plot and three replicates. The first factor corresponded to graywater irrigation depth equivalent to 25, 50, 75 and 100% of the available water content of the soil, and the second factor was the addition of bovine manure as fertilizer (0 and 34 Mg ha-1), and a control (irrigation with low-salinity water). Irrigation with graywater effluent did not promote adverse effects on gas exchanges and phytomass accumulation; however, it also did not provide enough nutrients to promote increase in these variables. The reduction in irrigation depth caused a decrease in gas exchange from 45 days after the application of the treatments. The basal tiller mass was the most favored plant component due to organic fertilization.
Key words:
Pennisetum glaucum; irrigation water depths; bovine manure; wastewater
RESUMO
A água cinza é um método alternativo para aumentar a oferta hídrica para produção agrícola nas regiões semiáridas. O objetivo deste estudo foi avaliar os efeitos de diferentes lâminas de irrigação de água cinza nas trocas gasosas e acúmulo de fitomassa do milheto com e sem adubação orgânica. A pesquisa foi conduzida em condições de casa de vegetação em Serra Talhada-PE, municipio na região semiárida do Brasil, em delineamento de blocos casualizados em esquema fatorial (4 × 2 + 1) e três repetições. O primeiro fator correspondeu à lâmina de irrigação com água cinza equivalente a 25, 50, 75 e 100% de água disponível do solo, e o segundo fator a adição de esterco bovino como fertilizante (0 e 34 Mg ha-1), e um controle (irrigação com água de baixa salinidade). A irrigação com efluente de água cinza não promove efeitos negativos nas trocas gasosas e acúmulo de fitomassa, contudo, também não disponibiliza nutrientes suficientes para incrementar essas variáveis. A redução das lâminas de irrigação causou diminuição das trocas gasosas a partir dos 45 dias após aplicação dos tratamentos. A massa de perfilhos basais foi o componente da planta mais favorecida pela adubação orgânica.
Palavras-chave:
Pennisetum glaucum; lâminas de irrigação; esterco bovino; água residuária
HIGHLIGHTS:
Higher gas exchange values during the initial growth stage are associated with significant phytomass accumulation in pearl millet.
Graywater did not provide enough nutrients to boost the millet phytomass accumulation.
Fertilization with bovine manure favored an increase in basal tiller mass.
Introduction
The irregularity of rainfall is the main factor limiting agricultural and livestock production in semi-arid regions. The use of wastewater for irrigation is a management strategy aimed to minimize the impact of water scarcity (Leonel & Tonetti, 2021Leonel, L. P.; Tonetti, A. L. Wastewater reuse for crop irrigation: Crop yield, soil and human health implications based on giardiasis epidemiology. Science of the Total Environment, v.775, p.145833, 2021. https://doi.org/10.1016/j.scitotenv.2021.145833
https://doi.org/10.1016/j.scitotenv.2021...
). In addition, it is a source of nutrients (Schaer et al., 2014Schaer, M. B.; Santos, M. E. P. dos; Medeiros, Y. D. P. Viabilidade do reúso de água como elemento mitigador dos efeitos da seca no semiárido da Bahia. Ambiente & Sociedade, v.17, p.17-32, 2014. https://doi.org/10.1590/S1414-753X2014000200003
https://doi.org/10.1590/S1414-753X201400...
). Among the wastewater types, graywater effluent is useful for agriculture as it does not receive waste from latrines; thus, it has a low content of organic matter (less risk of clogging) and pathogenic organisms (less chance of contamination) (Leong et al., 2017Leong, J. Y. C.; Oh, K. S.; Poh, P. E.; Chong, M. N. Prospects of hybrid rainwater-greywater decentralised system for water recycling and reuse: A review. Journal of Cleaner Production, v.142, p.3014-3027, 2017. https://doi.org/10.1016/j.jclepro.2016.10.167
https://doi.org/10.1016/j.jclepro.2016.1...
).
The amount of water applied via irrigation to crops also plays a significant role in optimizing water resources (Ismail et al., 2018Ismail, S. M.; El‐Nakhlawy, F. S.; Basahi, J. M. Sudan grass and pearl millets productivity under different irrigation methods with fully irrigation and stresses in arid regions. Grassland Science, v.64, p.29-39, 2018. https://doi.org/10.1111/grs.12179
https://doi.org/10.1111/grs.12179...
). However, a decrease in the volume of water applied to crops can cause disturbances in physiology (stomatal closure) and metabolism (accumulation of compatible osmolytes and production of reactive oxygen species [ROS]) in plants (Zhang et al., 2013Zhang, L.; Zhang, L.; Sun, J.; Zhang, Z.; Ren, H.; Sui, X. Rubisco gene expression and photosynthetic characteristics of cucumber seedlings in response to water deficit. Scientia Horticulturae, v.161, p.81-87, 2013. https://doi.org/10.1016/j.scienta.2013.06.029
https://doi.org/10.1016/j.scienta.2013.0...
; Chaves et al., 2016Chaves, M. M.; Costa, J. M.; Zarrouk, O.; Pinheiro, C.; Lopes, C. M.; Pereira, J. S. Controlling stomatal aperture in semi-arid regions - The dilemma of saving water or being cool? Plant Science, v.251, p.54-64, 2016. https://doi.org/10.1016/j.plantsci.2016.06.015
https://doi.org/10.1016/j.plantsci.2016....
). These alterations reduce CO2 uptake, slow down the Calvin cycle and interfere with plant growth (Liu et al., 2020Liu, F.; Fu, X.; Wu, G.; Feng, Y.; Li, F.; Bi, H.; Ai, X. Hydrogen peroxide is involved in hydrogen sulfide-induced carbon assimilation and photoprotection in cucumber seedlings. Environmental and Experimental Botany, v.175, p.104052, 2020. https://doi.org/10.1016/j.envexpbot.2020.104052
https://doi.org/10.1016/j.envexpbot.2020...
).
Millet [Pennisetum glaucum (L.) R. Br.] is characterized by adaptation to regions with low precipitation and high air temperatures (Nicolau Sobrinho et al., 2009Nicolau Sobrinho, W.; Santos, R. V. dos; Menezes Júnior, J. C.; Souto, J. S. Acúmulo de nutrientes nas plantas de milheto em função da adubação orgânica e mineral. Revista Caatinga, v.22, p.107-110, 2009.), demonstrating that it is a promising species for cultivation in places receiving wastewater. Millet can replace maize and sorghum in animal diets, with these latter species more demanding of water and nutrients than millet (Brunette et al., 2016Brunette, T.; Baurhoo, B.; Mustafa, A. F. Effects of replacing grass silage with forage pearl millet silage on milk yield, nutrient digestion, and ruminal fermentation of lactating dairy cows. Journal of Dairy Science, v.99, p.269-279. 2016. https://doi.org/10.3168/jds.2015-9619
https://doi.org/10.3168/jds.2015-9619...
).
Although wastewater contains dissolved nutrients, it does not provide adequate nutrients (Santos Júnior et al., 2015Santos Júnior, J. A.; Souza, C. F. de; Pérez-Marin, A. M.; Cavalcante, A. R.; Medeiros, S. de S. Interação urina e efluente doméstico na produção do milheto cultivado em solos do semiárido paraibano. Revista Brasileira de Engenharia Agrícola e Ambiental, v.19, p.456-463, 2015. https://doi.org/10.1590/1807-1929/agriambi.v19n5p456-463
https://doi.org/10.1590/1807-1929/agriam...
). The high costs of industrialized fertilizers and their effect on the environment have encouraged organic fertilizer research, which can improve the physical, chemical, and biological characteristics of the soil (Vimal et al., 2017Vimal, S. R.; Singh, J. S.; Arora, N. K.; Singh, S. Soil-plant-microbe interactions in stressed agriculture management: a review. Pedosphere, v.27, p.177-192, 2017. https://doi.org/10.1016/S1002-0160(17)60309-6
https://doi.org/10.1016/S1002-0160(17)60...
). The objective of the present study was to investigate the effects of different water regimes of wastewater (graywater effluent), on the gas exchange and accumulation of millet phytomass with and without organic fertilization.
Material and Methods
The experiment was conducted from September to November 2017, in a protected environment (greenhouse) at the Academic Unit of Serra Talhada, Universidade Federal Rural de Pernambuco, in the Brazilian semi-arid region (altitude: 429 m, latitude: 7°56’15” S and longitude: 38°18’45” W). According to Köppen’s classification, the climate pattern of the region is semi-arid, hot, and dry (BShw). The environmental conditions (daily averages) of the greenhouse during the experiment presented a mean air temperature of 30.09 ± 1.57 °C and a mean relative air humidity of 44.00 ± 5.48% (Figure 1).
Dynamics of air temperature and relative air humidity in the greenhouse during the experimental period
A randomized block design was adopted, in the factorial scheme 4 × 2 + 1 (control) with three replicates. The first factor was the irrigation depths with graywater effluent (25, 50, 75 and 100% of the available soil water [ASW]) and the second factor was organic fertilization (with and without application of bovine manure). The control received irrigation from the low-salinity urban supply (0.20 dS m-1) (chemical characteristics in Table 1) with an irrigation depth equivalent to 100% ASW and did not receive any fertilization.
Chemical analysis of graywater effluent (WW) and the urban supply water (WS) used in irrigation of millet
The graywater effluent was collected from a rural residence in Carnaíba, Pernambuco State, Brazil (chemical characteristics in Table 1), and originated from a system that captured and filtered water from the bathroom, kitchen, and laundry washing of the family’s residence. The filtration system consisted of two parts: a tank operated as a grease trap and a filter system formed by a superficial layer of charcoal and layers of coarse gravel, coarse sand, fine sand, and fine gravel that retained the larger fat particles, soap remnants, and organic materials in suspension that were not caught by the grease trap. Second, a tranquilizer tank where the water used for irrigation was captured.
The IPA-Buck-1 BF (P. glaucum) millet cultivar was sown in pots with a capacity of 18 dm3, which were filled with soil until reaching a bulk density of 1.30 kg dm-3. The soil was collected in the first 20 cm layer of a eutrophic Ta Haplic Cambisol and was sieved through a 4 mm mesh. The chemical and physical characteristics of the soil were 40.0 mg dm-3 of phosphorus, 43 mg dm-3 of iron, 0.68 cmolc dm-3 of potassium, 1.30 cmolc dm-3 of calcium, 0.27 cmolc dm-3 sodium, 1.0 cmolc dm-3 of hydrogen + aluminum, 0.88 dag kg-1 organic matter, 72.2% sand, 17.2% silt, and 10.5% clay, with pH of 7.1.
Bovine manure was added to the soil and homogenized for subsequent filling of the pots, with 645 g of manure added to each pot, equivalent to a dose of 34 Mg ha-1, which according to Nicolau Sobrinho et al. (2009Nicolau Sobrinho, W.; Santos, R. V. dos; Menezes Júnior, J. C.; Souto, J. S. Acúmulo de nutrientes nas plantas de milheto em função da adubação orgânica e mineral. Revista Caatinga, v.22, p.107-110, 2009.), is sufficient for the total growth of millet. The chemical characteristics of the bovine manure were 10.44 g kg-1 of nitrogen, 5.28 g kg-1 of phosphorus, 10.50 g kg-1 of potassium, 11.20 g kg-1 of calcium, 6.85 g kg-1 of magnesium, 113.29 g kg-1 of carbon, and carbon: nitrogen ratio of 11. The treatments did not receive mineral fertilization.
Soil moisture at field capacity (FC) was determined in the pots following the methodology described by Casaroli & Jong van Lier (2008Casaroli, D.; Jong van Lier, Q. Critérios para determinação da capacidade de vaso. Revista Brasileira de Ciência do Solo, v.32, p.59-66, 2008. https://doi.org/10.1590/S0100-06832008000100007
https://doi.org/10.1590/S0100-0683200800...
) to estimate the ASW. The moisture content at the permanent wilting point (PWP) was determined using undisturbed soil samples subjected to 15 atm in a Richards extraction chamber. The ASW was measured by subtracting the PWP from the FC moisture content. FC and PWP for soil without bovine manure were 0.18 and 0.03 g g-1, respectively, and were 0.20 and 0.05 g g-1, respectively, for soil with bovine manure.
Nine seeds were distributed per pot and placed at 2.0 cm depth. The stand formation period lasted until 15 days after crop emergence. All pots were irrigated daily using the urban supply to maintain the soil at FC. After this period, thinning was performed, leaving only one plant per pot. Then the different graywater effluent depths began based on the ASW (25, 50, 75, and 100% ASW). Irrigation occurred daily to replace the water mass lost through evapotranspiration, which was estimated by weighing the vessels (Casaroli & Jong van Lier, 2008Casaroli, D.; Jong van Lier, Q. Critérios para determinação da capacidade de vaso. Revista Brasileira de Ciência do Solo, v.32, p.59-66, 2008. https://doi.org/10.1590/S0100-06832008000100007
https://doi.org/10.1590/S0100-0683200800...
).
The experiment was conducted for 60 days after the beginning of the treatments. Every 15 days, after the application of the treatments, gas exchange at the leaf level was determined by measuring net CO2 assimilation (A), stomatal conductance (gs), intercellular CO2 concentration (Ci), and transpiration (E). For these determinations, a portable infrared gas analyzer (model Licor 6400XT) was used and was operated with artificial light (PAR) of 1000 µmol of photons m-2 s-1, ambient CO2 concentration (390 ± 3.2 μmol CO2), and chamber temperature of 28 °C. Observations were taken on the second fully expanded leaf, from top to bottom, between 8:00 and 11:00 a.m. after irrigation.
Using the gas exchange parameters, the instantaneous water use efficiency (A/E), intrinsic water use efficiency (A/gs), and instantaneous carboxylation efficiency (A/Ci) were estimated. Simultaneous with the gas exchange reading, the apparent electron transport rate (ETR) and the ratio between the ETR and net photosynthetic rate (ETR/A) were measured using a Licor 6400-40 modular fluorimeter.
At the end of the experiment, the following morphological components were collected and separated from the main tillers (largest growing tillers) and the basal tillers of the plants: live leaves, dead leaves, stem, and panicle. The material was dried in a forced-air ventilated oven at 65 °C until it reached a constant weight to determine the dry matter content.
Initially, the data were analyzed using the Shapiro-Wilk and Cochran homoscedasticity tests. Analysis of variance was conducted using the F test (p < 0.05) and the Tukey test (p < 0.05) to compare means, after which significant regression analysis was performed for quantitative factors (water fractions available in the soil). To compare the control treatment with those irrigated with graywater effluent (with and without organic fertilization), the Dunnett test (p < 0.05) was applied. R software (R Core Team, 2017R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2017. Available on: <Available on: https://www.r-project.org/ >. Accessed on: Mar. 2020.
https://www.r-project.org/...
) was used for data processing, figure creation, and statistical analysis.
Results and Discussion
From evaluation of gas exchanges at 15, 30, 45, and 60 days after the application of treatments (DAT), there was no interaction between treatments (irrigation depths and fertilization) for the simple effect of organic fertilization with or without bovine manure (Table 2). The differences between the control and treatments with and without organic fertilization are shown in Table 2.
At 15 DAT, the net CO2 assimilation (A) in the fertilized plants was 22 and 30% higher than that in plants without fertilization and the control, respectively (Table 2). Bovine manure fertilization increased the amount of nutrients in the soil solution, including nitrogen. An increase in the nitrogen availability to the plant promotes greater CO2 assimilation. Li et al. (2013Li, D.; Tian, M.; Cai, J.; Jiang, D.; Cao, W.; Dai, T. Effects of low nitrogen supply on relationships between photosynthesis and nitrogen status at different leaf position in wheat seedlings. Plant Growth Regulation, v.70, p.257-263, 2013. https://doi.org/10.1007/s10725-013-9797-4
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) stated that nitrogen increased the chlorophyll content in the leaves and activity of the chloroplasts.
The A did not differ between the control treatment and those irrigated with graywater for the other evaluation times (30, 45, and 60 DAT). At 30 and 45 DAT, A did not differ between treatments with and without fertilizer; however, a difference did occur at 60 DAT when A was higher in the treatment without fertilizer (Table 2). The A was higher when millet was in a balanced nutritional management, contributing to mitigating water stress and providing rapid initial growth (Kuwahara et al., 2016Kuwahara, F. A.; Souza, G. M.; Guidorizi, K. A.; Costa, C.; Meirelles, P. R. de L. Phosphorus as a mitigator of the effects of water stress on the growth and photosynthetic capacity of tropical C4 grasses. Acta Scientiarum. Agronomy, v.38, p.363-370, 2016. https://doi.org/10.4025/actasciagron.v38i3.28454
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). By obtaining higher gas exchanges at the beginning of growth, plants that received fertilization completed their cycle in a shorter period than plants without fertilization, justifying the drop in gas exchanges they exhibited at 60 DAT.
The stomatal conductance (gs) and transpiration (E) followed the same pattern as A when comparing the treatments with and without fertilization and irrigated with graywater effluent (Table 2). When gs and E were compared between the control treatment and those irrigated with graywater effluent (with and without fertilization), no statistical differences were observed at any time points (Table 2).
The plants in the control treatment showed the lowest intrinsic efficiency of water use at all assessment times (Table 2), probably due to low A without decreasing gs by the same magnitude. This tendency was also observed for the instantaneous water use efficiency. A lower water use efficiency implies a more significant loss of water to fix 1 g of CO2 (Comas et al., 2019Comas, L. H.; Trout, T. J.; DeJonge, K. C.; Zhang, H.; Gleason, S. M. Water productivity under strategic growth stage-based deficit irrigation in maize. Agricultural Water Management , v.212, p.433-440, 2019. https://doi.org/10.1016/j.agwat.2018.07.015
https://doi.org/10.1016/j.agwat.2018.07....
).
At 15, 30, 45 and 60 DAT, the intercellular concentration of CO2 (Ci) was higher in the control treatment than the treatments with and without organic fertilization (Table 2), which was possibly related to the lower A of the plants in the control treatment. Although A did not always differ between treatments, the A in the control treatment was always lower. The smaller the A, the greater the excess of CO2 in the leaf mesophyll (because since CO2 will not enter the Calvin cycle), consequently increasing the Ci (Liu et al., 2012Liu, M.; Qi, H.; Zhang, Z. P.; Song, Z. W.; Kou, T. J.; Zhang, W. J.; Yu, J. L. Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. African Journal of Agricultural Research, v.7, p.4750-4759, 2012. https://doi.org/10.5897/AJAR12.082
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).
The carboxylation efficiency (A/Ci) did not differ between treatments with and without fertilization at 15, 30, and 45 DAT. However, at 60 DAT, the A/Ci was higher in plants without fertilization. Therefore, the sharp drop in A at 60 DAT was probably related to the accelerated growth that millet had during the initial phase when fertilized, justifying the lower A/Ci found at 60 DAT. The control had lower A/Ci at 15 and 30 DAT; however, it was equal to the treatment without fertilization at 45 and 60 DAT, similar to the treatment with fertilization.
Most of the time, when A/Ci decreased, there was an increase in Ci. This increase in CO2 in the mesophyll indicated that the substrate for photosynthesis was available in the plant; however, the plant could not enter the Calvin cycle. Thus, as there were no limitations in the entry of CO2 into the leaf, the losses in A for the control treatment were associated with limitations in the photochemical phase (decrease in the supply of NADPH and ATP) or biochemical factors (regeneration and Rubisco carboxylation) (Galmés et al., 2011Galmés, J.; Ribas-Carbó, M.; Medrano, H.; Flexas, J. Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress. Journal of Experimental Botany, v.62, p.653-665, 2011. https://doi.org/10.1093/jxb/erq303
https://doi.org/10.1093/jxb/erq303...
; Mashilo et al., 2017Mashilo, J.; Odindo, A. O.; Shimelis, H. A.; Musenge, P.; Tesfay, S. Z.; Magwaza, L. S. Drought tolerance of selected bottle gourd [Lagenaria siceraria (Molina) Standl.] landraces assessed by leaf gas exchange and photosynthetic efficiency. Plant Physiology and Biochemistry , v.120, p.75-87, 2017. https://doi.org/10.1016/j.plaphy.2017.09.022
https://doi.org/10.1016/j.plaphy.2017.09...
).
The reduction in A/Ci increases the susceptibility to photochemical damage, because there is an excess of light energy at the photosystem II level due to low CO2 assimilation rates (Caemmerer & Furbank, 2016Caemmerer, S.; Furbank, R. T. Strategies for improving C4 photosynthesis. Current Opinion in Plant Biology, v.31, p.125-134, 2016. https://doi.org/10.1016/j.pbi.2016.04.003
https://doi.org/10.1016/j.pbi.2016.04.00...
). This was confirmed by the increasing ETR/A (dynamics similar to carboxylation efficiency), indicating electron deviation for other acceptors that were not A. These free electrons could bind with oxygen, forming reactive oxygen species, causing oxidative damage to plant cells, thus affecting plant metabolism (Mittler, 2002Mittler, R. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, v.7, p.405-410, 2002. https://doi.org/10.1016/S1360-1385(02)02312-9
https://doi.org/10.1016/S1360-1385(02)02...
).
The effects of the different irrigation levels were observed only at 45 and 60 DAT, indicating the tolerance of millet to water stress during early growth stages. The high frequency of irrigation (daily) might have compensated for the effect of water deficit on gas exchanges, aiding in the tolerance of millet during the early growth stages. Gas exchanges are affected more intensely when long irrigation intervals are adopted (Puértolas et al., 2020Puértolas, J.; Albacete, A.; Dodd, I. C. Irrigation frequency transiently alters whole plant gas exchange, water and hormone status, but irrigation volume determines cumulative growth in two herbaceous crops. Environmental and Experimental Botany, v.176, p.1-11, 2020. https://doi.org/10.1016/j.envexpbot.2020.104101
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). When the plants reached the stages that demanded more water (after 30 DAT), the frequency of irrigation and intrinsic tolerance of the crop were not adequate for overcoming the effect of deficit irrigation on gas exchange.
As the irrigation levels increased at 45 and 60 DAT, the A, E, and gs also increased (Figures 2A, B, and C). Irrigation with 25% ASW promoted a reduction of 30 and 38% in A at 45 and 60 DAT, respectively (Figure 2A). Under low water availability, plants control their stomatal opening (reduction of gas exchanges) to decrease water loss, resulting in a reduction in E and A, from which a cascade of effects on plant metabolism is initiated (Liu et al., 2012Liu, M.; Qi, H.; Zhang, Z. P.; Song, Z. W.; Kou, T. J.; Zhang, W. J.; Yu, J. L. Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. African Journal of Agricultural Research, v.7, p.4750-4759, 2012. https://doi.org/10.5897/AJAR12.082
https://doi.org/10.5897/AJAR12.082...
; Devi & Reddy, 2020Devi, M. J.; Reddy, V. R. Stomatal closure response to soil drying at different vapor pressure deficit conditions in maize. Plant Physiology and Biochemistry, v.154, p.714-722, 2020. https://doi.org/10.1016/j.plaphy.2020.07.023
https://doi.org/10.1016/j.plaphy.2020.07...
). These metabolic changes depend on the intensity of stress and the number of stressful events (Singh et al., 2021Singh, R. K.; Muthamilarasan, M.; Prasad, M. Biotechnological approaches to dissect climate-resilient traits in millets and their application in crop improvement. Journal of Biotechnology, v.37, p.64-73, 2021. https://doi.org/10.1016/j.jbiotec.2021.01.002
https://doi.org/10.1016/j.jbiotec.2021.0...
).
Gas exchanges of millet irrigated with different levels of wastewater (graywater effluent) at 45 and 60 days after application of the treatment (DAT): net CO2 assimilation - A (A), transpiration rate - E (B), stomatal conductance - gs (C) and intercellular CO2 concentration - Ci (D)
The E was reduced by 29 and 36% when millet was irrigated with 25% ASW at 45 and 60 DAT, respectively (Figure 2B). In addition, a 35% reduction in gs was observed when millet was irrigated with 25% ASW at 45 and 60 DAT (Figure 2C). Thus, plants exposed to water shortage conditions, first responded to maintain water status closure of the stomata, resulting in a reduction in stomatal conductance and transpiration (Chaves et al., 2016Chaves, M. M.; Costa, J. M.; Zarrouk, O.; Pinheiro, C.; Lopes, C. M.; Pereira, J. S. Controlling stomatal aperture in semi-arid regions - The dilemma of saving water or being cool? Plant Science, v.251, p.54-64, 2016. https://doi.org/10.1016/j.plantsci.2016.06.015
https://doi.org/10.1016/j.plantsci.2016....
).
Regardless of irrigation levels, the Ci in the leaf mesophyll did not fit any model satisfactorily at 45 DAT, and as water availability in the soil decreased at 60 DAT, Ci increased (Figure 2D). The increase in Ci under water scarcity indicates that the reduction in photosynthesis was not only caused by stomatal regulation (Liu et al., 2012Liu, M.; Qi, H.; Zhang, Z. P.; Song, Z. W.; Kou, T. J.; Zhang, W. J.; Yu, J. L. Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. African Journal of Agricultural Research, v.7, p.4750-4759, 2012. https://doi.org/10.5897/AJAR12.082
https://doi.org/10.5897/AJAR12.082...
). Thus, the reduction in A value with increased water deficiency (Figure 2A) was also due to dysfunctions in the levels of biochemical reactions associated with CO2 fixation, possibly due to limitations in the Rubisco synthesis caused by ATP deficiency (Mashilo et al., 2017Mashilo, J.; Odindo, A. O.; Shimelis, H. A.; Musenge, P.; Tesfay, S. Z.; Magwaza, L. S. Drought tolerance of selected bottle gourd [Lagenaria siceraria (Molina) Standl.] landraces assessed by leaf gas exchange and photosynthetic efficiency. Plant Physiology and Biochemistry , v.120, p.75-87, 2017. https://doi.org/10.1016/j.plaphy.2017.09.022
https://doi.org/10.1016/j.plaphy.2017.09...
).
The most drastic reduction in A was observed in the treatments with water deficiency at 60 DAT (Figure 2A) and was related to a decrease in the ETR (Figure 3A). The electron transport capacity is one of the main limiting mechanisms of CO2 assimilation (Caemmerer & Furbank, 2016Caemmerer, S.; Furbank, R. T. Strategies for improving C4 photosynthesis. Current Opinion in Plant Biology, v.31, p.125-134, 2016. https://doi.org/10.1016/j.pbi.2016.04.003
https://doi.org/10.1016/j.pbi.2016.04.00...
). The inability to transport electrons to supply reducers and ATP limits Rubisco’s regeneration (Zhang et al., 2013Zhang, L.; Zhang, L.; Sun, J.; Zhang, Z.; Ren, H.; Sui, X. Rubisco gene expression and photosynthetic characteristics of cucumber seedlings in response to water deficit. Scientia Horticulturae, v.161, p.81-87, 2013. https://doi.org/10.1016/j.scienta.2013.06.029
https://doi.org/10.1016/j.scienta.2013.0...
). Consequently, the net CO2 assimilation is affected. The reduction in irrigation depth at 45 and 60 DAT promoted an increase in the ETR/A (Figure 3B), indicating a surplus of electrons in the photosynthetic process. When these free electrons bind with O2, they form reactive oxygen species (ROS), promoting oxidative damage in plant cells (Mashilo et al., 2017Mashilo, J.; Odindo, A. O.; Shimelis, H. A.; Musenge, P.; Tesfay, S. Z.; Magwaza, L. S. Drought tolerance of selected bottle gourd [Lagenaria siceraria (Molina) Standl.] landraces assessed by leaf gas exchange and photosynthetic efficiency. Plant Physiology and Biochemistry , v.120, p.75-87, 2017. https://doi.org/10.1016/j.plaphy.2017.09.022
https://doi.org/10.1016/j.plaphy.2017.09...
). ROS production in thylakoids can also cause the deactivation of enzymes related to photosynthesis and inhibition of the functional activity of photosystem II (Zhang et al., 2013).
Effect of available water content in the electron transport rate (ETR) (A); indicative of electron drift (ETR/A) (B) and, carboxylation efficiency (A/Ci) (C) of millet plants at 45 and 60 days after application of the treatment (DAT) irrigated with different levels of wastewater (graywater effluent)
The carboxylation efficiency (A/Ci) was affected at 60 DAT due to the ASW, which increased proportionally with the irrigation levels (Figure 3C). The irrigation water regime did not influence the intrinsic and instantaneous water use efficiency due to the decrease in A, gs, and E being in the same magnitude as a function of the irrigation depth. Water use efficiency is an important mechanism of physiological adaptation, which can improve crop productivity under limited water availability (Bhattarai et al., 2020Bhattarai, B.; Singh, S.; West, C. P.; Ritchie, G. L.; Trostle, C. L. Water depletion pattern and water use efficiency of forage sorghum, pearl millet, and corn under water limiting condition. Agricultural Water Management, v.238, p.106-206, 2020. https://doi.org/10.1016/j.agwat.2020.106206
https://doi.org/10.1016/j.agwat.2020.106...
), and plants regulate their metabolism to continue assimilating CO2, with restrictions on transpiration.
The phytomass production (dry matter) of millet plants, regardless of the available water level in the soil, was higher for all fertilization treatments (Table 3). Therefore, graywater contains nutrients that cannot increase millet production. The amount of nutrients in the graywater effluent used in the experiment was related to the natural fertility of the soil used, which does not include inputs from residential latrines that, generally contribute to a large part of the nutrients in wastewater (Larsen & Lienert, 2001Larsen, T. A.; Lienert, J. Societal implications of re-engineering the toilet. Water Intelligence Online March, v.35, p.192-197, 2001. https://doi.org/10.1021/es012328d
https://doi.org/10.1021/es012328d...
; Santos Júnior et al., 2015Santos Júnior, J. A.; Souza, C. F. de; Pérez-Marin, A. M.; Cavalcante, A. R.; Medeiros, S. de S. Interação urina e efluente doméstico na produção do milheto cultivado em solos do semiárido paraibano. Revista Brasileira de Engenharia Agrícola e Ambiental, v.19, p.456-463, 2015. https://doi.org/10.1590/1807-1929/agriambi.v19n5p456-463
https://doi.org/10.1590/1807-1929/agriam...
). Human urine can represent more than 80% of the nitrogen found in domestic effluent, 50% of the phosphorus load, 90% of the potassium load, and less than 1% of the total volume of conventional domestic effluent (Larsen & Lienert, 2001).
According to Santos Júnior et al. (2015Santos Júnior, J. A.; Souza, C. F. de; Pérez-Marin, A. M.; Cavalcante, A. R.; Medeiros, S. de S. Interação urina e efluente doméstico na produção do milheto cultivado em solos do semiárido paraibano. Revista Brasileira de Engenharia Agrícola e Ambiental, v.19, p.456-463, 2015. https://doi.org/10.1590/1807-1929/agriambi.v19n5p456-463
https://doi.org/10.1590/1807-1929/agriam...
), the addition of 4.5% human urine to domestic effluent applied via irrigation in millet plants, resulted in dry mass and water use efficiency similar to those observed in plants under mineral fertilization and irrigation with municipal supply water. However, when human waste is present in wastewater, more advanced treatment techniques are required to avoid the risk of environmental and human contamination. This entails a higher cost for small farmers, which can make the reuse of wastewater economically unfeasible.
The additional cost of bovine manure fertilization is justified by increased production because since millet production was increased by more than 100% regardless of the irrigation level, when fertilized with bovine manure (Table 3). The production of millet plants irrigated with graywater effluent and without fertilization was not influenced by the irrigation regimes (Table 3). These same treatments did not differ from the control, which exhibited a dry matter production of 15.39 g plant-1.
However, plants fertilized and irrigated with 25% ASW differed from other treatments with fertilization, i.e., the phytomass production in the 50, 75 and 100% ASW treatments were 66, 53 and 63% higher than that in the 25% ASW treatments respectively (Table 3). Bovine manure fertilization accelerated the vegetative growth of millet during the early growth stages. However, when plants are exposed to water deficit, they suffer more from this stress because they have a more developed leaf mass, requiring more water (Uppal et al., 2015Uppal, R. K.; Wani, S. P.; Garg, K. K.; Alagarswamy, G. Balanced nutrition increases yield of pearl millet under drought. Field Crops Research, v.177, p.86-97, 2015. https://doi.org/10.1016/j.fcr.2015.03.006
https://doi.org/10.1016/j.fcr.2015.03.00...
).
Comparison of the phytomass accumulation of plants irrigated with graywater effluent and fertilized in the control treatment revealed increases of 102, 236, 209, 230 for 25, 50, 75, and 100% ASW, respectively. These results highlight the importance of organic fertilization for millet to achieve higher yields; even under the effect of water stress (25% ASW), the accumulation of phytomass was greater than that of the control.
At 45 and 60 DAT, A increased linearly with ASW (Figure 3A); however, the millet phytomass at 50, 75, and 100% ASW did not differ significantly. The frequency of irrigation directly influenced the biomass productivity of plants, and the shorter the time interval between the water application events, the lower the effect of the water deficit (Puértolas et al., 2020Puértolas, J.; Albacete, A.; Dodd, I. C. Irrigation frequency transiently alters whole plant gas exchange, water and hormone status, but irrigation volume determines cumulative growth in two herbaceous crops. Environmental and Experimental Botany, v.176, p.1-11, 2020. https://doi.org/10.1016/j.envexpbot.2020.104101
https://doi.org/10.1016/j.envexpbot.2020...
).
Organic fertilization benefited the dry mass of the basal tillers more than the mass of the principal tillers (Figure 4A). In fertilized treatments, the dry mass of basal tillers contributed to more than 50% of the total dry mass of the plant, whereas in the unfertilized treatments it contributed only 15% of the total dry mass. The proportion of live leaves was lower in the fertilized treatments (Figure 4B). Thus, the treatments that received more water and fertilization showed accelerated growth, as indicated by gas exchange (Table 2); consequently, a greater mass of dead leaves was observed when harvested in the advanced growth stages.
Partition of millet dry matter in main tillers and basal tillers (A) and plant partition in live leaves (LL), dead leaves (DL), stalk and panicle of millet plants (B) irrigated with graywater effluent and without and with organic fertilization (0 and 34 Mg ha-1 of bovine manure)
The fertilized treatments showed panicles in the basal tillers, contributing to the higher proportion of panicles in the dry mass of plants (Figure 4B), thus causing a better quality of forage, as the panicles have high starch content in the grains. The increase in the proportion of panicles is important to produce silage and higher amounts of organic acids (notably lactic acid), and increase the quality of millet silage (Brunette et al., 2016Brunette, T.; Baurhoo, B.; Mustafa, A. F. Effects of replacing grass silage with forage pearl millet silage on milk yield, nutrient digestion, and ruminal fermentation of lactating dairy cows. Journal of Dairy Science, v.99, p.269-279. 2016. https://doi.org/10.3168/jds.2015-9619
https://doi.org/10.3168/jds.2015-9619...
). The phytomass partition of the control treatment was similar to that of the treatment irrigated with 100% AWS of graywater effluent with no fertilization (Figure 4). This result highlighted that graywater did not promote harmful effects on millet production; further, it also did not increase the phytomass partition.
Conclusions
-
Wastewater (graywater effluent) did not negatively influence the phytomass production of millet. However, fertilization was required to achieve a high phytomass yield.
-
Irrigation with graywater effluent promoted an increase in carboxylation efficiency and intrinsic water use efficiency. While the fertilization with organic bovine manure favored an increase in gas exchange at 15 DAT.
-
The reduction in gas exchange after 45 DAT decreased the accumulation of millet phytomass in the fertilized plants and those irrigated with 25% of the available soil water.
-
The application of 50% of the available water to the soil fertilized with bovine manure promoted a more significant water saving without reducing phytomass accumulation.
-
The basal tillers mass of millet was the component most favored by organic fertilization.
Acknowledgements
This work is part of the National Observatory of Water and Carbon Dynamics in the Caatinga Biome - NOWCDCB, supported by FACEPE (Grant: APQ-0296-5.01/17; APQ-0498-3.07/17 NOWCDCB; APQ-0532-5.01/14) and CNPq (Processes: 435508/2018-0; 312984/2017-0). In addition, the first author (José Ralison I. Silva) thanks FACEPE support for granting a Master’s scholarship (IBPG-1786-5.01/16).
Literature Cited
- Bhattarai, B.; Singh, S.; West, C. P.; Ritchie, G. L.; Trostle, C. L. Water depletion pattern and water use efficiency of forage sorghum, pearl millet, and corn under water limiting condition. Agricultural Water Management, v.238, p.106-206, 2020. https://doi.org/10.1016/j.agwat.2020.106206
» https://doi.org/10.1016/j.agwat.2020.106206 - Brunette, T.; Baurhoo, B.; Mustafa, A. F. Effects of replacing grass silage with forage pearl millet silage on milk yield, nutrient digestion, and ruminal fermentation of lactating dairy cows. Journal of Dairy Science, v.99, p.269-279. 2016. https://doi.org/10.3168/jds.2015-9619
» https://doi.org/10.3168/jds.2015-9619 - Caemmerer, S.; Furbank, R. T. Strategies for improving C4 photosynthesis. Current Opinion in Plant Biology, v.31, p.125-134, 2016. https://doi.org/10.1016/j.pbi.2016.04.003
» https://doi.org/10.1016/j.pbi.2016.04.003 - Casaroli, D.; Jong van Lier, Q. Critérios para determinação da capacidade de vaso. Revista Brasileira de Ciência do Solo, v.32, p.59-66, 2008. https://doi.org/10.1590/S0100-06832008000100007
» https://doi.org/10.1590/S0100-06832008000100007 - Chaves, M. M.; Costa, J. M.; Zarrouk, O.; Pinheiro, C.; Lopes, C. M.; Pereira, J. S. Controlling stomatal aperture in semi-arid regions - The dilemma of saving water or being cool? Plant Science, v.251, p.54-64, 2016. https://doi.org/10.1016/j.plantsci.2016.06.015
» https://doi.org/10.1016/j.plantsci.2016.06.015 - Comas, L. H.; Trout, T. J.; DeJonge, K. C.; Zhang, H.; Gleason, S. M. Water productivity under strategic growth stage-based deficit irrigation in maize. Agricultural Water Management , v.212, p.433-440, 2019. https://doi.org/10.1016/j.agwat.2018.07.015
» https://doi.org/10.1016/j.agwat.2018.07.015 - Devi, M. J.; Reddy, V. R. Stomatal closure response to soil drying at different vapor pressure deficit conditions in maize. Plant Physiology and Biochemistry, v.154, p.714-722, 2020. https://doi.org/10.1016/j.plaphy.2020.07.023
» https://doi.org/10.1016/j.plaphy.2020.07.023 - Galmés, J.; Ribas-Carbó, M.; Medrano, H.; Flexas, J. Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress. Journal of Experimental Botany, v.62, p.653-665, 2011. https://doi.org/10.1093/jxb/erq303
» https://doi.org/10.1093/jxb/erq303 - Ismail, S. M.; El‐Nakhlawy, F. S.; Basahi, J. M. Sudan grass and pearl millets productivity under different irrigation methods with fully irrigation and stresses in arid regions. Grassland Science, v.64, p.29-39, 2018. https://doi.org/10.1111/grs.12179
» https://doi.org/10.1111/grs.12179 - Kuwahara, F. A.; Souza, G. M.; Guidorizi, K. A.; Costa, C.; Meirelles, P. R. de L. Phosphorus as a mitigator of the effects of water stress on the growth and photosynthetic capacity of tropical C4 grasses. Acta Scientiarum. Agronomy, v.38, p.363-370, 2016. https://doi.org/10.4025/actasciagron.v38i3.28454
» https://doi.org/10.4025/actasciagron.v38i3.28454 - Larsen, T. A.; Lienert, J. Societal implications of re-engineering the toilet. Water Intelligence Online March, v.35, p.192-197, 2001. https://doi.org/10.1021/es012328d
» https://doi.org/10.1021/es012328d - Leonel, L. P.; Tonetti, A. L. Wastewater reuse for crop irrigation: Crop yield, soil and human health implications based on giardiasis epidemiology. Science of the Total Environment, v.775, p.145833, 2021. https://doi.org/10.1016/j.scitotenv.2021.145833
» https://doi.org/10.1016/j.scitotenv.2021.145833 - Leong, J. Y. C.; Oh, K. S.; Poh, P. E.; Chong, M. N. Prospects of hybrid rainwater-greywater decentralised system for water recycling and reuse: A review. Journal of Cleaner Production, v.142, p.3014-3027, 2017. https://doi.org/10.1016/j.jclepro.2016.10.167
» https://doi.org/10.1016/j.jclepro.2016.10.167 - Li, D.; Tian, M.; Cai, J.; Jiang, D.; Cao, W.; Dai, T. Effects of low nitrogen supply on relationships between photosynthesis and nitrogen status at different leaf position in wheat seedlings. Plant Growth Regulation, v.70, p.257-263, 2013. https://doi.org/10.1007/s10725-013-9797-4
» https://doi.org/10.1007/s10725-013-9797-4 - Liu, F.; Fu, X.; Wu, G.; Feng, Y.; Li, F.; Bi, H.; Ai, X. Hydrogen peroxide is involved in hydrogen sulfide-induced carbon assimilation and photoprotection in cucumber seedlings. Environmental and Experimental Botany, v.175, p.104052, 2020. https://doi.org/10.1016/j.envexpbot.2020.104052
» https://doi.org/10.1016/j.envexpbot.2020.104052 - Liu, M.; Qi, H.; Zhang, Z. P.; Song, Z. W.; Kou, T. J.; Zhang, W. J.; Yu, J. L. Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. African Journal of Agricultural Research, v.7, p.4750-4759, 2012. https://doi.org/10.5897/AJAR12.082
» https://doi.org/10.5897/AJAR12.082 - Mashilo, J.; Odindo, A. O.; Shimelis, H. A.; Musenge, P.; Tesfay, S. Z.; Magwaza, L. S. Drought tolerance of selected bottle gourd [Lagenaria siceraria (Molina) Standl.] landraces assessed by leaf gas exchange and photosynthetic efficiency. Plant Physiology and Biochemistry , v.120, p.75-87, 2017. https://doi.org/10.1016/j.plaphy.2017.09.022
» https://doi.org/10.1016/j.plaphy.2017.09.022 - Mittler, R. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, v.7, p.405-410, 2002. https://doi.org/10.1016/S1360-1385(02)02312-9
» https://doi.org/10.1016/S1360-1385(02)02312-9 - Nicolau Sobrinho, W.; Santos, R. V. dos; Menezes Júnior, J. C.; Souto, J. S. Acúmulo de nutrientes nas plantas de milheto em função da adubação orgânica e mineral. Revista Caatinga, v.22, p.107-110, 2009.
- Puértolas, J.; Albacete, A.; Dodd, I. C. Irrigation frequency transiently alters whole plant gas exchange, water and hormone status, but irrigation volume determines cumulative growth in two herbaceous crops. Environmental and Experimental Botany, v.176, p.1-11, 2020. https://doi.org/10.1016/j.envexpbot.2020.104101
» https://doi.org/10.1016/j.envexpbot.2020.104101 - R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2017. Available on: <Available on: https://www.r-project.org/ >. Accessed on: Mar. 2020.
» https://www.r-project.org/ - Santos Júnior, J. A.; Souza, C. F. de; Pérez-Marin, A. M.; Cavalcante, A. R.; Medeiros, S. de S. Interação urina e efluente doméstico na produção do milheto cultivado em solos do semiárido paraibano. Revista Brasileira de Engenharia Agrícola e Ambiental, v.19, p.456-463, 2015. https://doi.org/10.1590/1807-1929/agriambi.v19n5p456-463
» https://doi.org/10.1590/1807-1929/agriambi.v19n5p456-463 - Schaer, M. B.; Santos, M. E. P. dos; Medeiros, Y. D. P. Viabilidade do reúso de água como elemento mitigador dos efeitos da seca no semiárido da Bahia. Ambiente & Sociedade, v.17, p.17-32, 2014. https://doi.org/10.1590/S1414-753X2014000200003
» https://doi.org/10.1590/S1414-753X2014000200003 - Singh, R. K.; Muthamilarasan, M.; Prasad, M. Biotechnological approaches to dissect climate-resilient traits in millets and their application in crop improvement. Journal of Biotechnology, v.37, p.64-73, 2021. https://doi.org/10.1016/j.jbiotec.2021.01.002
» https://doi.org/10.1016/j.jbiotec.2021.01.002 - Uppal, R. K.; Wani, S. P.; Garg, K. K.; Alagarswamy, G. Balanced nutrition increases yield of pearl millet under drought. Field Crops Research, v.177, p.86-97, 2015. https://doi.org/10.1016/j.fcr.2015.03.006
» https://doi.org/10.1016/j.fcr.2015.03.006 - Vimal, S. R.; Singh, J. S.; Arora, N. K.; Singh, S. Soil-plant-microbe interactions in stressed agriculture management: a review. Pedosphere, v.27, p.177-192, 2017. https://doi.org/10.1016/S1002-0160(17)60309-6
» https://doi.org/10.1016/S1002-0160(17)60309-6 - Zhang, L.; Zhang, L.; Sun, J.; Zhang, Z.; Ren, H.; Sui, X. Rubisco gene expression and photosynthetic characteristics of cucumber seedlings in response to water deficit. Scientia Horticulturae, v.161, p.81-87, 2013. https://doi.org/10.1016/j.scienta.2013.06.029
» https://doi.org/10.1016/j.scienta.2013.06.029
-
1 Research developed at Universidade Federal Rural de Pernambuco, Unidade Acadêmica de Serra Talhada, Serra Talhada, PE, Brazil
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Publication Dates
-
Publication in this collection
14 Jan 2022 -
Date of issue
Feb 2022
History
-
Received
03 May 2021 -
Accepted
01 Aug 2021 -
Published
01 Sept 2021