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The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco.

Valente MA, Faria JA, Soares-Ramos JR, Reis PA, Pinheiro GL, Piovesan ND, Morais AT, Menezes CC, Cano MA, Fietto LG, Loureiro ME, Aragão FJ, Fontes EP - J. Exp. Bot. (2008)

Bottom Line: When plants growing in soil were exposed to drought (by reducing or completely withholding watering) the wild-type lines showed a large decrease in leaf water potential and leaf wilting, but the leaves in the transgenic lines did not wilt and exhibited only a small decrease in water potential.It had previously been reported that tobacco BiP overexpression or repression reduced or accentuated the effects of drought.It is concluded that BiP overexpression confers resistance to drought, through an as yet unknown mechanism that is related to ER functioning.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Bioquímica e Biologia Molecular, BIOAGRO, Universidade Federal de Viçosa, Avenida PH Rolfs s/n, 36571.000 Viçosa, MG, Brazil.

ABSTRACT
The ER-resident molecular chaperone BiP (binding protein) was overexpressed in soybean. When plants growing in soil were exposed to drought (by reducing or completely withholding watering) the wild-type lines showed a large decrease in leaf water potential and leaf wilting, but the leaves in the transgenic lines did not wilt and exhibited only a small decrease in water potential. During exposure to drought the stomata of the transgenic lines did not close as much as in the wild type, and the rates of photosynthesis and transpiration became less inhibited than in the wild type. These parameters of drought resistance in the BiP overexpressing lines were not associated with a higher level of the osmolytes proline, sucrose, and glucose. It was also not associated with the typical drought-induced increase in root dry weight. Rather, at the end of the drought period, the BiP overexpressing lines had a lower level of the osmolytes and root weight than the wild type. The mRNA abundance of several typical drought-induced genes [NAC2, a seed maturation protein (SMP), a glutathione-S-transferase (GST), antiquitin, and protein disulphide isomerase 3 (PDI-3)] increased in the drought-stressed wild-type plants. Compared with the wild type, the increase in mRNA abundance of these genes was less (in some genes much less) in the BiP overexpressing lines that were exposed to drought. The effect of drought on leaf senescence was investigated in soybean and tobacco. It had previously been reported that tobacco BiP overexpression or repression reduced or accentuated the effects of drought. BiP overexpressing tobacco and soybean showed delayed leaf senescence during drought. BiP antisense tobacco plants, conversely, showed advanced leaf senescence. It is concluded that BiP overexpression confers resistance to drought, through an as yet unknown mechanism that is related to ER functioning. The delay in leaf senescence by BiP overexpression might relate to the absence of the response to drought.

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Related in: MedlinePlus

Elevated levels of BiP confer drought tolerance to soybean plants under a restricted water regime. (A) Overexpression of BiP maintains leaf turgidity under drought. Drought stress was induced by reducing irrigation to 40% of the daily normal water supply. The leaves were photographed on day 18 of the experiment. (B) Leaf water potential of transgenic leaves under drought stress (reducing daily irrigation). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type. I, normally irrigated; DS, drought stress. (C, D, E) Photosynthesis and water relations in soybean transgenic lines continuously irrigated or exposed to the drought regime. Photosynthetic rate (C), stomatal conductance (D), and transpiration rate (E) of the third fully expanded leaf of WT and transgenic lines (as indicated) were measured by the LI-6400 infrared (IR) gas analyser at 1000 μmol m−2 s−1 irradiance. I, control leaves (normal irrigation). DS, leaves after 18 d of drought stress (40% of normal daily irrigation). After 18 d under the restricted water regime, the plants were rewatered with a normal water supply for 5 d (RW-5d) or 14 d (RW-5d). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type.
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fig2: Elevated levels of BiP confer drought tolerance to soybean plants under a restricted water regime. (A) Overexpression of BiP maintains leaf turgidity under drought. Drought stress was induced by reducing irrigation to 40% of the daily normal water supply. The leaves were photographed on day 18 of the experiment. (B) Leaf water potential of transgenic leaves under drought stress (reducing daily irrigation). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type. I, normally irrigated; DS, drought stress. (C, D, E) Photosynthesis and water relations in soybean transgenic lines continuously irrigated or exposed to the drought regime. Photosynthetic rate (C), stomatal conductance (D), and transpiration rate (E) of the third fully expanded leaf of WT and transgenic lines (as indicated) were measured by the LI-6400 infrared (IR) gas analyser at 1000 μmol m−2 s−1 irradiance. I, control leaves (normal irrigation). DS, leaves after 18 d of drought stress (40% of normal daily irrigation). After 18 d under the restricted water regime, the plants were rewatered with a normal water supply for 5 d (RW-5d) or 14 d (RW-5d). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type.

Mentions: To investigate whether overexpression of BiP was correlated with water stress tolerance in soybean transgenic lines, either T3 transgenic plants at the V6 developmental stage or T4 transgenic plants at the V3 developmental stage were subjected to two distinct water deficit regimes, slow and fast soil drying treatments. In the first one, water deficit was induced by a reduction of irrigation to a 40% level for 18 d. This slow soil drying experiment was intended to mimic field conditions and to allow physiological and molecular responses to low water potential (ψw) be examined for a longer period. The soil water content of all samples was recorded as a function of time to ensure that the extent of soil drying or the severity of plant water stress was similar for all samples analysed. After 18 d of 40% irrigation the leaves of wild-type plants had completely wilted. The transgenic plants, by contrast, had normal turgid leaves (Fig. 2A). The leaf ψw of stressed wild-type plants declined to a maximum stress of –2.2 MPa, whereas the leaf ψw of transgenic plants did not decrease below –0.7 to –1.0 MPa (Fig. 2B). The leaf water status indicated that BiP overexpressing lines were protected against dehydration. However, this was not a direct result of stomatal closure because, in independent transgenic lines under stress conditions, the stomatal conductance and transpiration rate were significantly higher than in wild-type lines (Fig. 2D, E). The stomatal conductance, transpiration and photosynthetic rate did not differ in well-watered wild-type and transgenic lines (Fig. 2C, D, E). The transgenic lines also displayed normal growth and were undistinguible from the wild type (results not shown). However, under 40% irrigation the stomata did not close as much as in the wild type, and both the rate of transpiration and the rate of photosynthesis were not reduced as much as in the wild type (Fig. 2C). In the 40% irrigation experiment, the photochemical efficiency (Fv/Fm ratio) of transgenic and wild-type leaves remained unaltered and was similar to that of the well-watered counterparts (data not shown). After the 18 d period of drought, the plants were rewatered and their recovery was evaluated (Fig. 2). By contrast with the wild-type plants that required 14 d to recover (RW-14d), the transgenic lines recovered faster. Within a 5 d period of normal watering, their rate of photosynthesis and transpiration, and their stomatal conductance were similar to that of continuously normally irrigated controls. By then these parameters had significantly higher values than in the drought-stressed wild type.


The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco.

Valente MA, Faria JA, Soares-Ramos JR, Reis PA, Pinheiro GL, Piovesan ND, Morais AT, Menezes CC, Cano MA, Fietto LG, Loureiro ME, Aragão FJ, Fontes EP - J. Exp. Bot. (2008)

Elevated levels of BiP confer drought tolerance to soybean plants under a restricted water regime. (A) Overexpression of BiP maintains leaf turgidity under drought. Drought stress was induced by reducing irrigation to 40% of the daily normal water supply. The leaves were photographed on day 18 of the experiment. (B) Leaf water potential of transgenic leaves under drought stress (reducing daily irrigation). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type. I, normally irrigated; DS, drought stress. (C, D, E) Photosynthesis and water relations in soybean transgenic lines continuously irrigated or exposed to the drought regime. Photosynthetic rate (C), stomatal conductance (D), and transpiration rate (E) of the third fully expanded leaf of WT and transgenic lines (as indicated) were measured by the LI-6400 infrared (IR) gas analyser at 1000 μmol m−2 s−1 irradiance. I, control leaves (normal irrigation). DS, leaves after 18 d of drought stress (40% of normal daily irrigation). After 18 d under the restricted water regime, the plants were rewatered with a normal water supply for 5 d (RW-5d) or 14 d (RW-5d). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2651463&req=5

fig2: Elevated levels of BiP confer drought tolerance to soybean plants under a restricted water regime. (A) Overexpression of BiP maintains leaf turgidity under drought. Drought stress was induced by reducing irrigation to 40% of the daily normal water supply. The leaves were photographed on day 18 of the experiment. (B) Leaf water potential of transgenic leaves under drought stress (reducing daily irrigation). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type. I, normally irrigated; DS, drought stress. (C, D, E) Photosynthesis and water relations in soybean transgenic lines continuously irrigated or exposed to the drought regime. Photosynthetic rate (C), stomatal conductance (D), and transpiration rate (E) of the third fully expanded leaf of WT and transgenic lines (as indicated) were measured by the LI-6400 infrared (IR) gas analyser at 1000 μmol m−2 s−1 irradiance. I, control leaves (normal irrigation). DS, leaves after 18 d of drought stress (40% of normal daily irrigation). After 18 d under the restricted water regime, the plants were rewatered with a normal water supply for 5 d (RW-5d) or 14 d (RW-5d). Each value represents the mean ±SD of five replicates from three independent experiments. The asterisks indicate significant differences at P ≤0.05 as compared to the wild type.
Mentions: To investigate whether overexpression of BiP was correlated with water stress tolerance in soybean transgenic lines, either T3 transgenic plants at the V6 developmental stage or T4 transgenic plants at the V3 developmental stage were subjected to two distinct water deficit regimes, slow and fast soil drying treatments. In the first one, water deficit was induced by a reduction of irrigation to a 40% level for 18 d. This slow soil drying experiment was intended to mimic field conditions and to allow physiological and molecular responses to low water potential (ψw) be examined for a longer period. The soil water content of all samples was recorded as a function of time to ensure that the extent of soil drying or the severity of plant water stress was similar for all samples analysed. After 18 d of 40% irrigation the leaves of wild-type plants had completely wilted. The transgenic plants, by contrast, had normal turgid leaves (Fig. 2A). The leaf ψw of stressed wild-type plants declined to a maximum stress of –2.2 MPa, whereas the leaf ψw of transgenic plants did not decrease below –0.7 to –1.0 MPa (Fig. 2B). The leaf water status indicated that BiP overexpressing lines were protected against dehydration. However, this was not a direct result of stomatal closure because, in independent transgenic lines under stress conditions, the stomatal conductance and transpiration rate were significantly higher than in wild-type lines (Fig. 2D, E). The stomatal conductance, transpiration and photosynthetic rate did not differ in well-watered wild-type and transgenic lines (Fig. 2C, D, E). The transgenic lines also displayed normal growth and were undistinguible from the wild type (results not shown). However, under 40% irrigation the stomata did not close as much as in the wild type, and both the rate of transpiration and the rate of photosynthesis were not reduced as much as in the wild type (Fig. 2C). In the 40% irrigation experiment, the photochemical efficiency (Fv/Fm ratio) of transgenic and wild-type leaves remained unaltered and was similar to that of the well-watered counterparts (data not shown). After the 18 d period of drought, the plants were rewatered and their recovery was evaluated (Fig. 2). By contrast with the wild-type plants that required 14 d to recover (RW-14d), the transgenic lines recovered faster. Within a 5 d period of normal watering, their rate of photosynthesis and transpiration, and their stomatal conductance were similar to that of continuously normally irrigated controls. By then these parameters had significantly higher values than in the drought-stressed wild type.

Bottom Line: When plants growing in soil were exposed to drought (by reducing or completely withholding watering) the wild-type lines showed a large decrease in leaf water potential and leaf wilting, but the leaves in the transgenic lines did not wilt and exhibited only a small decrease in water potential.It had previously been reported that tobacco BiP overexpression or repression reduced or accentuated the effects of drought.It is concluded that BiP overexpression confers resistance to drought, through an as yet unknown mechanism that is related to ER functioning.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Bioquímica e Biologia Molecular, BIOAGRO, Universidade Federal de Viçosa, Avenida PH Rolfs s/n, 36571.000 Viçosa, MG, Brazil.

ABSTRACT
The ER-resident molecular chaperone BiP (binding protein) was overexpressed in soybean. When plants growing in soil were exposed to drought (by reducing or completely withholding watering) the wild-type lines showed a large decrease in leaf water potential and leaf wilting, but the leaves in the transgenic lines did not wilt and exhibited only a small decrease in water potential. During exposure to drought the stomata of the transgenic lines did not close as much as in the wild type, and the rates of photosynthesis and transpiration became less inhibited than in the wild type. These parameters of drought resistance in the BiP overexpressing lines were not associated with a higher level of the osmolytes proline, sucrose, and glucose. It was also not associated with the typical drought-induced increase in root dry weight. Rather, at the end of the drought period, the BiP overexpressing lines had a lower level of the osmolytes and root weight than the wild type. The mRNA abundance of several typical drought-induced genes [NAC2, a seed maturation protein (SMP), a glutathione-S-transferase (GST), antiquitin, and protein disulphide isomerase 3 (PDI-3)] increased in the drought-stressed wild-type plants. Compared with the wild type, the increase in mRNA abundance of these genes was less (in some genes much less) in the BiP overexpressing lines that were exposed to drought. The effect of drought on leaf senescence was investigated in soybean and tobacco. It had previously been reported that tobacco BiP overexpression or repression reduced or accentuated the effects of drought. BiP overexpressing tobacco and soybean showed delayed leaf senescence during drought. BiP antisense tobacco plants, conversely, showed advanced leaf senescence. It is concluded that BiP overexpression confers resistance to drought, through an as yet unknown mechanism that is related to ER functioning. The delay in leaf senescence by BiP overexpression might relate to the absence of the response to drought.

Show MeSH
Related in: MedlinePlus