Gas exchange and yield response to foliar phosphorus application in Phaseolus vulgaris L. under drought

Resposta das trocas gasosas e da produtividade à aplicação foliar de fósforo em Phaseolus vulgaris L. sob seca

RESEARCH ARTICLE

Gas exchange and yield response to foliar phosphorus application in Phaseolus vulgaris L. under drought

Resposta das trocas gasosas e da produtividade à aplicação foliar de fósforo em Phaseolus vulgaris L. sob seca

Mauro Guida dos SantosI, ^*; Rafael Vasconcelos Ribeiro^I; Ricardo Ferraz de Oliveira^I; Carlos Pimentel^II

^ILaboratório de Fisiologia de Plantas sob Estresse, Departamento de Ciências Biológicas, Escola Superior de Agricultura "Luiz de Queiroz", Universidade de São Paulo, CP 09, CEP 13418-900, Piracicaba, SP, Brasil

^IIDepartamento de Fitotecnia, Instituto de Agronomia, Universidade Federal Rural do Rio de Janeiro, CEP 23851-970, Itaguaí, RJ, Brasil

ABSTRACT

This study was conducted to evaluate the effect of foliar Pi application on gas exchange and yield of bean genotypes submitted to a mild water deficit at the pre-flowering stage. In the first experiment, when extra Pi (10 g.L^-1) was sprayed on leaves during water stress or during recovery, there was no effect on gas exchange or yield in the A320, Carioca and Ouro Negro genotypes. However, net CO₂ assimilation (A) of A320 and Ouro Negro was less affected, but not significantly, than Carioca at the end of the stress, when Pi was supplied five days before water deficit. In the second experiment, two different doses of Pi (10 and 20 g.Pi L^-1) were sprayed five days before water deficit on the Carioca genotype. During the last three days of the mild water deficit, A values were significantly higher for the Pi20 treatment when compared to the control plants without extra Pi supply. The intrinsic water use efficiency for plants receiving Pi20 was significantly higher than for the other treatments. In addition, seed dry weight per plant was higher for plants receiving Pi20 dose than for plants with Pi10 and its control.

Key words: common bean, inorganic phosphorus, photosynthesis, water deficit.

RESUMO

Este estudo foi conduzido para avaliar o efeito do suprimento extra de fósforo foliar nas trocas gasosas e produção de genótipos de feijoeiro submetidos a déficit hídrico moderado no estádio de pré-floração. No primeiro experimento, quando o suprimento extra de fósforo (10 g.L^-1) foi aplicado durante o estresse hídrico ou na recuperação, não houve efeito significativo sobre as trocas gasosas ou produção nos genótipos A320, Carioca e Ouro Negro. Contudo, a assimilação líquida de CO₂ (A) de A320 e Ouro Negro foi menos afetada, mas não significativamente, que o Carioca no final do período de estresse, quando o Pi foi suprido cinco dias antes do déficit hídrico. No segundo experimento, duas doses diferentes de Pi (10 e 20 g.L^-1) foram aplicadas cinco dias antes do início da seca no genótipo Carioca. Nos últimos três dias da deficiência hídrica moderada, os valores de A foram significativamente maiores para o tratamento Pi20 quando comparado às plantas-controle sem suprimento extra de Pi. A eficiência intrínseca do uso da água das plantas que receberam Pi20 foi significativamente maior em relação aos outros tratamentos. Além disso, o peso seco de sementes por planta foi maior nas plantas do tratamento Pi20.

Palavras-chave: déficit hídrico, feijão, fósforo inorgânico, fotossíntese.

INTRODUCTION

Common bean (Phaseolus vulgaris L.) is an important food crop grown under natural conditions in Latin America, where drought is one of the major limiting factors for plant production (Rosales-Serna et al., 2004). Drought effects can be enhanced when water stress occurs at specific phenological stages, such as pollination (Pimentel et al., 1999a), decreasing yield by more than 50 % (Norman et al., 1995). Neverthless, the common bean is considered very sensitive to environmental stresses (Magalhães and Millar, 1978; Pimentel et al., 1999b). According to Westgate and Boyer (1986), the low yield of water-stressed plants at the pollination stage is more related to an indirect effect of water deficit on photosynthesis than to a direct effect on pollination itself. At this stage, net CO₂ assimilation rate (A) is increased (Pimentel et al., 1999b), leading to greater leaf carbohydrate reserves, which can then sustain embryo growth after pollination (Kramer and Boyer, 1995; Schussler and Westgate, 1995).

Under drought, the photosynthetic rate can be limited by stomatal and non-stomatal factors (Chaves et al., 2004). Lauer and Boyer (1992) and Tang et al. (2002) suggested that metabolic factors are the main limitation in leaves under low water potential. Under water deficit conditions mechanisms are necessary to avoid plant dehydration (Jones, 1985; Laffray and Loughet, 1990). Therefore, reduced stomatal conductance and biochemical impairment are common resopnses of water-stressed plants. The latter is a photosynthetic metabolism reduction due to decreased chloroplast ability to regenerate RuBP (Flexas and Medrano, 2002). The intrinsic water use efficiency (IWUE), i.e., the rate of CO₂ assimilation obtained for a given stomatal conductance (A/g_s), can be considered a relevant index for selection of water deficit tolerant plants, mostly among C₃ species (Osmond et al., 1980), such as bean (Pimentel et al., 1999b).

Water deficit has a direct effect on the stomatal and enzymatic apparatus, as well as a long-term influence on uptake and shoot accumulation of phosphorus by crops (Mouatt and Nes, 1986), especially for a poor inorganic phosphate (Pi) extractor, such as bean (Fageria et al., 1997). Phosphorus is an important element that is also required for photosynthetic energy production and carbohydrate transport (Alam, 1999; Raghothama, 1999). In view of the Pi and triose-P antiport system present in chloroplast membranes, a decreased sink demand for sucrose can causes either an increase in starch synthesis or a reduction in CO₂ assimilation, both of which can be a consequence of low Pi recycling in the cytoplasm (Stitt and Quick, 1989; Holbrook and Keys, 2003). Lawlor and Cornic (2002) have reported that an inadequate Pi supply to the chloroplast can limit ATP synthesis. Pi supply to the chloroplast is crucial for maintaining phosphorylation reactions during CO₂ assimilation, when Pi is released from phosphorylated carbohydrates in the cytosol as a consequence of sucrose synthesis and export to other tissues (Leegood, 1996). Hendrickson et al. (2004), studying detached grapevine leaves under low temperature stress, found a large stimulation of photosynthetic O₂ evolution by feeding Pi to the leaves.

Therefore, low cytoplasmatic free Pi levels induced by water deficit, associated with leaf accumulation of sugars-P, can limit crop productivity by reducing the triose-P exchange rate between chloroplast and cytosol (Pieters et al., 2001). The effect can be enhanced at the pollination stage, when leaf carbohydrate content will be crucial for reproductive growth and, thus, for yield (Westgate and Boyer, 1986; Wardlaw, 1990). The hypothesis tested in this study was that extra Pi supply may alleviate the limitation induced by drought stress on bean photosynthesis, when supplied as a foliar spray.

MATERIALS AND METHODS

Plant material and growth condition: The genotypes of Phaseolus vulgaris L. A320 (a line that maintains high leaf water potential under drought condition; Pimentel et al., 1991), Carioca (a genotype widely used by farmers, Vicente et al., 2000) and Ouro Negro (a new black seeded cultivar) were used in this study. The plants were grown in 10 L pots (one plant per pot) with 8 kg of vermiculite (Plantimax — Eucatex Inc., Brazil). All the genotypes flowered at same time. Pots were arranged in a completely randomized block design, using 108 pots (3 genotypes x 2 foliar spray levels x 3 Pi supply dates x 2 irrigation regimes x 3 replications) in the first experiment, and 32 pots (1 genotype x 4 foliar spray levels x 2 irrigation regimes x 4 replications) in the second experiment. The experiments were conducted in a greenhouse where minimum and maximum air temperature varied from 10ºC to 33ºC and 12ºC to 38 ºC during the first and second experiments respectively. Pots were fertilized with K₂O (30 kg.ha^-1), P₂O₅ (90 kg.ha^-1) and dolomitic lime (1,500 kg.ha^-1), as proposed by Raij (1997), and also with micronutrients (300 mL of Hoagland's solution) according to McCree (1986). Before sowing, seeds were inoculated with Rhizobium leguminosarum biovar phaseoli (EMBRAPA/CNPAB, Brazil). Additional fertilizer was applied 25 days after seedling emergency (DAE), using soluble urea (40 kg N.ha^-1), as proposed by Vieira (1998). In both experiments, plants were watered regularly before imposing a water deficit. Irrigation was discontinued when genotypes were at the pre-flowering stage. After the water deficit treatment, the plants were rehydrated up to the end of their cycle.

Water deficit and foliar phosphorus supplementation treatments: In the first experiment, the three genotypes (A320, Carioca and Ouro Negro) were submitted to water withholding for 11 days at the pre-flowering stage (34 days after sowing). The plants were rehydrated when the predawn leaf water potential (Y_l) was around -0.9 MPa, which is considered a mild drought stress for common beans (Vassey and Sharkey, 1989). In the first experiment three different treatments for the extra Pi foliar supply were applied: in the first, the foliar Pi spray was applied five days before withholding irrigation (Y_l around -0.2 MPa); in the second, foliar Pi supply was sprayed when Y_l was around -0.4 MPa (on the sixth day of water deficit); and in the third, the foliar Pi spray was applied on the day of rehydration (11^th day of water deficit).

In the second experiment, only the genotype Carioca (genotype indicated for semi-arid areas or for use in breeding programs for drought tolerance) was used and the two different Pi doses were applied five days before water deficit. Water was withheld at the pre-flowering stage (34 days after sowing) for 10 days, and plants were rehydrated when Y_l was around -0.7 MPa, which characterizes a mild water deficit.

Phosphorus foliar supply and leaf phosphorus content: The treatment with extra Pi supply in both experiments was done by spraying leaves with a solution containing ammonium dihydrogen phosphate ((NH₄)H₂PO₄). Control plants were supplied with urea to balance the effect of nitrogen applied in Pi-supplied plants. In the first experiment, only one Pi concentration was used (10 g Pi.L^-1), and the control plants were sprayed with 2.64 g N.L^-1. All solutions were prepared according to Teixeira and Araújo (1999). In the second experiment, two Pi concentrations were used: Pi10 (10 g Pi.L^-1) and Pi20 (20 g Pi.L^-1). There were two control treatments in this second experiment: N10 (2.64 g N.L^-1) and N20 (5.28 g N.L^-1). Leaf phosphorus content was assayed (Malavolta et al., 1997) at day zero of the water deficit, for a leaf at the same position and age as those used for gas exchange measurements.

Gas exchange, leaf water potential and yield components: Measurements of net CO₂ assimilation rate (A) and stomatal conductance (g_s) were taken with an infra-red gas analyzer (IRGA), using an open system with a 6 cm² clamp-on leaf cuvette (LI-6400, LICOR, Lincoln, NE, USA). The middle leaflet of the third trifoliolate leaf, which was the youngest fully expanded leaf, was used for gas exchange measurements. The gas exchange system was zeroed daily using CO₂-free air.

In the first experiment, gas exchange measurements were done between 09:00 and 10:30 h, under a photosynthetic photon flux density (PPFD) of 800 mmol.m^-2.s^-1. The other microclimate conditions prevailing in the leaf cuvette were the same as the outside atmosphere. In the second experiment, the gas exchange measurements were done between 09:00-10:30 h, 12:00-13:30 h and 15:00-16:30 h, under a PPFD of 500, 1000 and 600 µmol.m^-2.s^-1, respectively. These PPFD values are natural sunlight at the moment of the measurements, so these values were natural sunlight at the moment of the measurements. In both experiments, the air CO₂ concentration inside the leaf cuvette was around 370 µmol.mol^-1.

The intrinsic water use efficiency (IWUE) was calculated by the relationship A/g_s (Osmond et al., 1980). The pre-dawn tension in the xylem was measured daily with a Scholander pressure chamber (Soilmoisture Equipment Corp., Santa Barbara, CA, USA), for the fourth trifoliolate leaf from the base of the plant, which was a mature but not senescent leaf. These measurements were assumed to measure the leaf water potential (Y_l). At the end of the cycle of the plants, the effects of both water deficit and extra Pi supply were evaluated on plant yield components: seed weight per plant and number of pods per plant.

Statistical analysis: Data were subjected to analysis of variance (ANOVA), and means were compared by the Tukey test at 0.05 of probability, when significance was detected.

RESULTS

Effects of foliar phosphorus supply at different dates (first experiment): On the 11^th day after suspending irrigation (figure 1), when plants were watered for recovery, the predawn leaf water potential (Y_l) was around -0.9 MPa, which corresponds to a mild water deficit for bean (Sharkey and Seemann, 1989). In this experiment, supplying extra Pi did not significantly affect Y_l among genotypes. In addition, stomatal conductance (g_s) was not significantly affected by extra Pi supply or genotypes under drought (data not shown), but g_s was reduced on the 11^th day of water stress by 92 %, 90 %, and 94 % for A320, Carioca, and Ouro Negro respectively, when compared with the well-watered plant (data not shown). Net CO₂ assimilation (A) of A320 and Ouro Negro was less affected, but not significantly, when Pi was supplied five days before water deficit. In this Pi supply treatment, both genotypes showed higher A than Carioca on the 8^th and 10^th day of water stress (figures 2A and 2G). Also, Carioca exhibited higher A values when Pi was supplied during water shortage (figure 2E). Almost all Pi-supplied genotypes showed higher A values on recovery for all treatments, especially when Pi was supplied five days prior drought (figures 2A, 2D and 2G).

In the first experiment, extra Pi supply on the last day of water deficit (11^th day) had no significant effect on A for any genotype (figures 2C, 2F and 2I). Although Pi-supplied plants had shown increased A during and/or after the water deficit period, extra Pi supply did not improved yield components for any treatment (data not shown).

Effects of foliar phosphorus concentrations (second experiment): In the second essay, Y_l of the genotypes decreased during water deficit to a value of around -0.7 MPa on 10^th day (figure 3). As in the first experiment, there was no significant effect for extra Pi supply on gas exchange of well-watered plants and in g_s of water-stressed plants (data not shown). Nevertheless, Pi20-supplied and stressed leaves exhibited higher A values (p<0.05) at 09:00 h on days six, eight and ten of water deficit (figure 4D), and at 12:00 h from days eight to ten of stress (figures 4D and 4E) and the second day of rehydration (figure 4E). The IWUE on the last day of drought (10^th day of stress) at 15:00 h was higher for Pi20-supplied leaves (p<0.01) than for the other treatments (Pi10, N10, and N20), as shown in table 2. Considering yield components of Pi-supplied and water-stressed Carioca plants, seed dry weight was higher in Pi20 treatment (table 3).

DISCUSSION

Drought stress can decrease the Pi uptake from soil (Mouatt and Nes, 1986), reducing the availability of leaf Pi for the Pi/triose-P translocator resulting in impaired chloroplast photoassimilatory metabolism (Leegood, 1996; Flügge et al., 2003). At the same time, an increase in photosynthetic phosphorylated intermediates may occur in the cytoplasm and vacuoles, which represents an additional limitation to the photosynthetic metabolism. Extra foliar Pi supply for well-watered plants did not affect A over the first four days of measurements (data not shown). This was probably due to continued growth and photoassimilate export in well-watered plants, maintaining the vacuolar and cytosolic Pi reservs (Sivak and Walker, 1986; Mimura, 2001).

During the mild water deficit in the first experiment (plants were rehydrated when Y_l was around -0.9 MPa) when A320, Carioca and Ouro Negro genotypes were at the pre-flowering stage, no significant effect of foliar Pi spray was found on Y_l , g_s and A. The lowest Y_l values of Ouro Negro under maximum water stress (figures 1A, 1B and 1C) can be due to the non-conservative stomatal behaviour of this genotype, that is, lower IWUE values for Ouro Negro compared to Carioca and A320, as reported by Pimentel et al. (1999a). Also, the genotype A320 needs further studies with Pi supplied before water stress, because it has a lower stomatal conductance than other bean cultivars under drought (Pimentel et al., 1991; Pimentel el al., 1999a).

Extra Pi supply induced changes in photosynthetic rate only when it was sprayed before drought. During water stress, extra foliar Pi may not be absorbed preventing its utilization by cellular metabolism. When extra Pi was supplied at rehydration, there was a probable recovery of growth and photoassimilate export from mildly water-stressed leaves (Boyer, 1978), inducing Pi release from sugars-P compounds accumulated during stress. On the other hand, in the first experiment, the lack of an effect for extra Pi supplied before water stress can also be a consequence of low Pi spray concentration (table 1).

In general, beans have two main mechanisms for adapting to water deficit: stomatal control (Laffray and Louguet, 1990; Pimentel et al., 1999b) and root development (Kuruvadi and Aguilera, 1990). Although there was no effect of Pi supply on g_s of water-stressed bean plants, higher A values were found under water deficit in plants supplied with Pi20 solution (figures 4D, 4E and 4F) as well as higher IWUE values (p<0.01) in Pi20-supplied plants under maximum drought stress (table 2). Therefore, reduced g_s in a photosynthetically efficient genotype can decrease leaf transpiration, improving IWUE and maintaining plant growth and yield (Ehleringer, 1990; Pimentel et al., 1999a). As pointed out by Pimentel et al. (1999a), high IWUE values under water deficit, especially at the pollination stage, can be a useful physiological parameter for screening drought tolerance in bean breeding programs. Under low Y_l one factor reducing CO₂ availability in the chloroplast during drought might be stomatal closure (Chaves et al., 2004). However, loss of photosynthetic biochemical activity also seems to be involved (Lauer and Boyer, 1992; Tang et al., 2002).

The results show an alleviation of drought effects on A (figures 4D and 4F) by foliar Pi20 supply, increasing foliar Pi content (table 1) and seed dry weight in plants (p<0.05) (table 3). Under water deficit, Mouatt and Nes (1986) and Alam (1999) reported a low leaf Pi status of water-stressed plants due to reduced Pi uptake from soil. Since there was high leaf Pi content in Pi-supplied plants (table 3), it can be suggested that Pi is one of the factors inducing high A values in stressed-plants, especially with Pi20 concentration (figures 4D, 4E and 4F). In an elegant study with detached grapevine leaves, Hendrickson et al. (2004) found a great influence of Pi supply (47 to 80 %) on photosynthetic metabolism under low temperature stress.

For all plants, water stress caused reductions in pod number and seed dry weight per plant (table 3). The production of beans can be decreased by more than 50 % when water deficit occurs during the pollination or flowering stages (Norman et al., 1995; Pimentel et al., 1999a, b). These negative drought consequences in plant yield were reduced in Pi20-supplied plants, where a smaller decrease in pod number (20 %) and seed dry weight (26 %) was found compared with Pi10 (47 and 43 %, respectively), N10 (37 and 49.5 %, respectively) and N20 (37 and 43 %, respectively) supplied plants. However, more studies are necessary in order to understand the alleviation of photosynthetic metabolism and yield in common bean genotypes under water deficit, when they are supplied with extra foliar Pi.

Acknowledgements: M.G. Santos is grateful to CAPES (Comissão de Aperfeiçoamento de Pessoal de Nível Superior, Brazil), R.V. Ribeiro to FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil), and C. Pimentel to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil) for fellowships granted. We also thank Dr. E. Malavolta and C. Cabral for helpful support concerning foliar phosphorus concentration.

Received: 17/09/2004, Accepted: 25/11/2004

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Publication Dates

• Publication in this collection
  14 Feb 2005
• Date of issue
  Dec 2004

History

• Accepted
  25 Nov 2004
• Received
  17 Sept 2004