Scholarly article on topic 'Overcompensation or limitation to photosynthesis and root hydraulic conductance altered by rehydration in seedlings of sorghum and maize'

Overcompensation or limitation to photosynthesis and root hydraulic conductance altered by rehydration in seedlings of sorghum and maize Academic research paper on "Agriculture, forestry, and fisheries"

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{"Adaptive mechanism" / Dehydration / Recovery / "Hydraulic traits" / Rehydration}

Abstract of research paper on Agriculture, forestry, and fisheries, author of scientific article — Nan Wang, Jing Gao, Suiqi Zhang

Abstract In view of the prospect of irregular extremes of high and low rainfall due to climate change, the mechanisms underlying plant responses to periods of drought and re-watering need to be understood. Sorghum (Sorghum bicolor L.) and maize (Zea mays L.) were grown in pots of loess soil at three soil moisture levels to examine the effects of different levels of drought over 10days and plant responses to re-watering (5days of rehydration). Photosynthesis-related traits recovered rapidly both in sorghum and maize on re-watering, suggesting that photosynthetic function was not severely damaged after a short drought period, although the values of these traits were dramatically reduced during drought per se. However, the two species differed in the extent to which they recovered from severe stress. In sorghum, net photosynthetic rate (P n), stomatal conductance (G s), and maximum photochemical efficiency of PSII (F v/F m) returned to control levels after re-watering. However, in maize, these parameters exceeded control levels after re-watering. Both overcompensation and pre-drought limitation were observed. Over a range of growth conditions, close relationships between G s and root hydraulic conductance (K r) were observed in pooled data sets. P n, K r, and their related characteristics were compared among species and treatments. Our results showed that the recovery of K r is similar between sorghum and maize, at least after a short time of re-watering, although the two species differ in drought-tolerance capacity. Our results also suggest that sorghum can endure moderate drought by adjusting certain traits, but is still as vulnerable as maize under severe drought stress.

Academic research paper on topic "Overcompensation or limitation to photosynthesis and root hydraulic conductance altered by rehydration in seedlings of sorghum and maize"

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The Crop Journal

Overcompensation or limitation to photosynthesis and root hydraulic conductance altered by rehydration in seedlings of sorghum and maize^

Nan Wang a'c'*, Jing Gao b, Suiqi Zhangc

a Shaanxi Collaborative Innovation Center of Chinese Medicinal Resources Industrialization, Shaanxi University of Chinese Medicine, Xianyang 712083, China b College of Pharmacy, Shaanxi University of Chinese Medicine, Xianyang 712046, China c Institute of Soil and Water Conservation, Northwest A&F University, Yangling712100, China

ARTICLE INFO ABSTRACT

In view of the prospect of irregular extremes of high and low rainfall due to climate change, the mechanisms underlying plant responses to periods of drought and re-watering need to be understood. Sorghum (Sorghum bicolor L.) and maize (Zea mays L.) were grown in pots of loess soil at three soil moisture levels to examine the effects of different levels of drought over 10 days and plant responses to re-watering (5 days of rehydration). Photosynthesis-related traits recovered rapidly both in sorghum and maize on re-watering, suggesting that photosynthet-ic function was not severely damaged after a short drought period, although the values of these traits were dramatically reduced during drought perse. However, the two species differed in the extent to which they recovered from severe stress. In sorghum, net photosynthetic rate (Pn), stomatal conductance (Gs), and maximum photochemical efficiency of PSII (Fv/Fm) returned to control levels after re-watering. However, in maize, these parameters exceeded control levels after re-watering. Both overcompensation and pre-drought limitation were observed. Over a range of growth conditions, close relationships between Gs and root hydraulic conductance (Kr) were observed in pooled data sets. Pn, Kr, and their related characteristics were compared among species and treatments. Our results showed that the recovery of Kr is similar between sorghum and maize, at least after a short time of re-watering, although the two species differ in drought-tolerance capacity. Our results also suggest that sorghum can endure moderate drought by adjusting certain traits, but is still as vulnerable as maize under severe drought stress.

© 2017 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Article history:

Received 28 November 2016 Received in revised form 11 January 2017 Accepted 20 January 2017 Available online xxxx

Keywords:

Adaptive mechanism Dehydration Recovery Hydraulic traits Rehydration

1. Introduction

Soil conditions in agriculture are highly variable [1]. Irregular extremes of high and low rainfall, perhaps exacerbated by climatic changes, lead to soil water content alternating between drought and saturation in rainfed agriculture [2]. Such soil moisture fluctuations adversely affect crop growth, especially in regions without adequate irrigation. As climatic change is expected to become more pronounced, an understanding of the mechanisms that underlie plant adaptation and plasticity under extremes of soil moisture conditions is a research priority [3].

Plants are sensitive to sudden environmental changes such as decreased soil water content, and depend upon stress adaptations to survive or yield a crop [4]. To deal with water deficits, plants intensify their

☆ Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.

* Corresponding author at: Shaanxi Collaborative Innovation Center of Chinese Medicinal Resources Industrialization, Shaanxi University of Chinese Medicine, Xianyang 712083, China

E-mail address: gosouth@hotmail.com (N. Wang).

ability to acquire and/or conserve water under drought conditions, such as by making osmotic and metabolic pathway adjustments [5]. Damaged enzyme activities and mitochondrial oxidative properties can be restored upon re-watering magnitude and irreversible damage can be maintained at a low level during rehydration [6]. Furthermore, extraordinarily rapid plant growth can be observed when sufficient water is resupplied after dehydration [7]. In short, many studies have focused on the adaptive responses of plants to drought, whereas relatively few have demonstrated the capacity of plants to recover after re-watering and the accompanying changes in physiological and morphological processes [8].

Root hydraulic characteristics play an important role in plant drought adaptation [9]. Root hydraulic conductance (Kr), an indicator of the ease with which water is taken up by roots and transported to the shoot system, can be reduced under drought stress as a consequence of changes in the anatomical structure of the root, the root surface area, and root permeability [10]. Therefore, the recovery of Kr following drought can be expected to play an important role in adaptation to soil moisture fluctuations [11]. Previous studies have demonstrated the relationships between Kr and several plant traits [12], but have neglected to demonstrate the extent to which these relationships may

http://dx.doi.org/mi 016/j.cj.2017.01.005

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change when plants are rehydrated after drought stress. Furthermore, the extent of plant recovery can be limited by the intensity and duration of the preceding drought before rehydration [13]. This phenomenon is called "pre-drought limitation". In addition, when water is resupplied, plants can sometimes undergo overcompensatory growth that offsets the losses caused by previous drought stress [14]. Both overcompensa-tion and pre-drought limitation have been observed in previous rehy-dration experiments [15]. Thus, our understanding of these relationships can usefully be extended through additional research in which duration and intensity of drought is considered in relation to recovery. These relationships relate directly to the irregular rainfall cycles increasingly experienced in practical farming.

Sorghum (Sorghum bicolor L.) is commonly cultivated in water-deficient environments. Although innate features of sorghum make this crop suitable for drought regions, further studies of drought tolerance and recovery after re-watering under changeable environmental conditions are needed. Maize (Zea mays L.) is susceptible to mild drought and its growth can be dramatically affected by unfavorable soil water conditions, especially at the seedling stage [16]. To compare the mechanisms of recovery between the two species, pot experiments were conducted with the following aims: (1) to determine whether recovery responses are consistent between sorghum and maize, (2) to determine which morphological or physiological characteristics are coordinated with root hydraulic traits during drought stress and re-watering, and (3) to determine whether sorghum and maize display overcompensation or pre-drought limitation after re-watering.

2. Materials and methods

Pot experiments were performed at the Northwest A&F University, Yangling (34.27°N, 108.07°E), Shaanxi Province in the semi-arid Loess Plateau. The loess soil used (pH 8.2) contained 2.7 g kg-1 organic matter, 11.2 mg kg-1 available N, 6.6 mg kg-1 available P, and 94.9 mg kg-1 available K and showed a field waterholding capacity of 20%. The sorghum cultivar Jinza 4 and the maize cultivar Hudan 4 were sown in plastic pots (14 cm in diameter and 17 cm in height) at room temperature (25 °C) and subsequently transplanted into plastic buckets at the 5-leaf seedling stage (one seedling per bucket). Each bucket (28.6 cm in diameter and 27.5 cm in height) contained 13 kg of air-dried soil.

The following treatments and associated soil relative water contents were used: (1) CK (control), 75% ± 5% of field waterholding capacity; (2) MS (moderate stress), 55% ± 5% of field waterholding capacity; and (3) SS (severe stress), 35% ± 5% of field waterholding capacity. The relative soil water content was regulated according to weight. The pots were daily weighed and re-watered at 18:00. A vertical plastic pipe was placed adjacent to the inner wall to supply water from the bottom of the pot. The soil water treatments were initiated at the 8-leaf seedling stage and maintained for a period of 10 days. After 10 days, all drought treatments were re-watered to the CK treatment level.

Leaf gas exchange was measured on the third leaf from the top of each plant using the Portable Photosynthesis System Li-6400 (LI-COR, Inc., Lincoln, Nebraska, USA) between 9:30 and 11:00 a.m. The settings were 1300 ^mol m-2 s-1 light intensity, 65% ± 5% relative humidity, 35 °C leaf temperature, and 380 ^mol mol-1 CO2. The data were collected on two occasions: after 10 days of drought and again after five days of re-watering.

The leaves were detached from the plants and used for the chlorophyll fluorescence assay. The maximum photochemical efficiency of PSII (Fv/Fm) was analyzed using the IMAGING-PAM M-Series Chlorophyll Fluorescence System (Heinz-Walz, Effeltrich, Germany). The leaves were dark-adapted for 30 min prior to obtaining the measurements and saturation pulses were generated every 20 s.

Kr is defined as the rate of water flow (mg s-1) per unit pressure drop (MPa) driving flow through the entire root system. It was measured using a high-pressure flow meter (HPFM) (Dynamax Inc., Houston, TX, USA) as described by detail in Tyree et al. [17]. The device

injects pressurized water into the roots and uses the linear relationship between pressure and water flow to calculate hydraulic conductance. The shoots were excised from the roots (c. 5 cm above the soil), and a watertight container was constructed around the base of each plant. The HPFM was attached to the root system, and 3-6 "transient" flow measurements were immediately obtained. During each measurement, the pressure was increased from 0 to 0.05 MPa at a rate of 3-7 kPa s-1, and the instantaneous flow was measured every 3 s. The entire sequence of flow measurements was completed after approximately 10 min. The flow was plotted against the applied pressure driving the flow into the root system, and the hydraulic conductance was then calculated from the slope of the linear regression.

Root surface area (Ar) and total root length (RL) were calculated using WinRHIZO Pro STD4800 software (Regent Instruments Inc., Quebec, Canada). Total leaf area (A) was geometrically calculated from the length and width measurements [18].

All measurements were repeated three times using three independent plants. The data were analyzed using the statistical package SPSS 13 (SPSS Inc., Chicago, IL, USA). One-way analysis of variance (ANOVA) followed by the Least Significant Difference Test (LSD) in the post hoc analysis was applied to compare the treatment means. The treatment effects were considered to be significant at P < 0.05.

3. Results

Photosynthetic parameters, including Pn (net photosynthetic rate), Gs (stomatal conductance) and Fv/Fm, decreased markedly under both applied drought stresses in seedlings of sorghum and maize compared with their values under the CK condition (Fig. 1). After rehydration, Pn, Gs, and Fv/Fm of sorghum that underwent two different drought stresses both recovered gradually to CK levels (Fig. 1). Although Pn, Gs, and Fv/Fm of maize under MS and SS conditions also recovered to CK levels after re-watering, the values of Pn, Gs, and Fv/Fm of maize experiencing the SS condition significantly exceeded CK levels on day four of re-watering (Fig. 1).

Based on pooled data, close relationships between Gs and Kr were observed over a range of growth conditions (Fig. 2). Pn, E, RL, Ar, and Al showed no significant relationships with Kr under pooled data analysis (Fig. 2). The data were then divided into two groups: sorghum and maize. Pn, Gs, and Ar of sorghum showed significant relationships with Kr (Fig. 3). Al and Ar of maize showed significant relationships with Kr (Fig. 3). RL and Al of sorghum and Pn and RL of maize showed marginally significant relationships with Kr (Fig. 3).

Under MS and SS conditions, drought stress reduced Kr, Ar, Al, and RL of maize compared with CK (Table 1). Under SS conditions, drought stress reduced Kr, Ar, Al, and RL of sorghum compared with CK (Table 1). Under MS conditions, Kr of sorghum slightly exceeded CK levels with no significant difference and Ar, Al, and RL of sorghum showed no significant difference with CK (Table 1). After re-watering, the measured values for both sorghum and maize experiencing the SS condition increased but did not recover to the CK levels except for Al and RLof maize (Table 1).

Both overcompensation and pre-drought limitation were observed after a short period of re-watering (Fig. 1). In sorghum, Pn, Gs, and Fv/ Fm of CK were higher than the corresponding values of MS and SS during the whole experiment (Fig. 1), showing pre-drought limitation. Pn, Gs, and Fv/Fm of maize under SS conditions were higher than those of CK and MS at the late stage of rehydration (Fig. 1), showing overcompensation.

4. Discussion

Drought stress has been reported to severely depress photosynthesis and stomatal opening [19]. In the present study, the reduction levels in Gs and Pn of sorghum and maize reflected the intensity of the imposed drought stress as well as the reduced opening of stomatal

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Fig. 1. Dynamic responses of net photosynthetic rate (Pn), stomatal conductance (Gs), and maximum photochemical efficiency of PSII (Fv/Fm) to re-watering are shown for sorghum and maize. CK: 75% ± 5% of field waterholding capacity; MS: 55% ± 5% of field waterholding capacity; SS: 35% ± 5% of field waterholding capacity. D11: after 10 days of drought stress; D11R1 -R5: after 1,2,3,4, and 5 days of re-watering. Means with different letters are significantly different at P < 0.05. Mean ± SE, n = 3.

apertures (Fig. 1). Photosynthetic rates were reduced under drought stress, but fully recovered following rehydration [20]. Mulberry plants regained nearly full functional capacities after 48 h of re-watering under different degrees of drought stress [21]. In the

present study, after re-watering, Pn under two different drought stress conditions eventually recovered to control levels (Fig. 1). Re-watering after drought stress leads to the full recovery of Pn, accompanied by the resumption of photosynthesis and the opening of

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Fig. 2. Relationships between root hydraulic conductance (Kr) and (A) net photosynthetic rate (Pn), (B) stomatal conductance (Gs), (C) transpiration rate (E), (D) root surface area (Ar),and (E) total leaf area (Al) in pooled data sets. CK represents no drought; D11 represents 10 days of drought stress; D11R5 represents after 10 days of drought stress and five days of re-watering.

stomatal apertures [15]. In the present study, Pn, Gs, and Fv/Fm quickly recovered in both crops after re-watering (Fig. 1). Photochemistry is sensitive to drought stress, and dehydration can damage the photosystem II reaction center (PS II) [22]. The maximum photochemical efficiency of PS II (Fv/Fm) can be used to detect PS II damage, as a decrease in Fv/Fm is indicative of the downregulation of photosynthesis [23]. The recovery rates of Fv/Fm (Fig. 1) indicate that although the values of these plant parameters are dramatically reduced by

drought, the photosynthesis apparatus is not markedly damaged under either MS or SS stress in a short period.

Over a range of growth conditions, close relationships between Gs and Kr were observed in pooled data sets (Fig. 2). Decreased Kr could reduce leaf water potential, resulting in stomatal closure [24]. The observation that both Kr and Gs recovered after re-watering (Fig. 1 and Table 1) further confirms the close relationship between Kr and Gs. However, in contrast to the results with pooled data sets, RL, Al,

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Fig.3. Relationships between root hydraulic conductance (Kr) and (A) net photosynthetic rate (Pn), (B) stomatal conductance (Gs), (C) transpiration rate (E), (D) root surface area (Ar),and (E) total leaf area (Ai) in separate groups (group 1: sorghum; group 2: maize). CK represents no drought; D11 represents 10 days of drought stress; D11R5 represents the 5th day of re-watering.

and Ar of both sorghum and maize showed correlations with Kr in the separate groups (Fig. 3). In other words, Kr increased with increasing RL, Al, and Ar (Fig. 3 and Table 1). Soil moisture fluctuations lead to changes in morphological and physiological traits of root that can cause corresponding changes in Kr [10]. Furthemore, a previous study also showed that decreased hydraulic conductance of root system can limit leaf expansion, total root length, and root dry weight [25].

In the present study, Kr of sorghum and maize significantly decreased under SS conditions (Table 1). In contrast, the Kr of sorghum under the MS condition was not reduced, but the Kr of maize significantly decreased under MS condition (Table 1). These results reflect the differing drought endurance capacities and response modes to water-availability conditions of plant species even when water deficit is mild [19]. Increased root length and higher solute concentrations are considered to be the reasons that sorghum has greater water absorbing

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Table 1

Changes over time in root hydraulic conductance (Kr), root surface area (Ar), total leaf area (Ai), and total root length (RL) of sorghum and maize.

Kr (mg s 1 MPa-1) Ar (m2) Al (m2) RL (m)

D11 D11R5 D11 D11R5 D11 D11R5 D11 D11R5

Sorghum

CK 2.50 ± 0.050 a 7.79 ± 0.341 a 0.58 ± 0.056 a 0.72 ± 0.060 a 0.14 ± 0.006 a 0.15 ± 0.003 a 101.12 ± 2.778 a 109.80 ± 0.722 a

MS 3.20 ± 0.332 a 5.89 ± 0.396 b 0.48 ± 0.029 ab 0.69 ± 0.033 a 0.13 ± 0.001 a 0.14 ± 0.001 ab 104.84 ± 2.188 a 110.47 ± 2.999 a

SS 1.09 ± 0.260 b 3.48 ± 0.123 c 0.39 ± 0.030 b 0.51 ± 0.020 b 0.11 ± 0.002 b 0.13 ± 0.007 b 92.57 ± 2.120 b 99.22 ± 1.722 b

CK 7.67 ± 0.206 a 8.52 ± 0.029 a 0.16 ± 0.001 a 0.17 ± 0.003 a 0.38 ± 0.011 a 0.38 ± 0.010 a 87.13 ± 3.653 a 107.66 ± 12.926 a

MS 5.70 ± 0.070 b 6.70 ± 0.218 b 0.14 ± 0.002 b 0.15 ± 0.005 b 0.36 ± 0.002 b 0.37 ± 0.016 a 79.60 ± 2.756 ab 103.93 ± 14.009 a

SS 3.15 ± 0.167 c 5.47 ± 0.115 c 0.09 ± 0.002 c 0.11 ± 0.001 c 0.32 ± 0.010 c 0.39 ± 0.024 a 73.98 ± 0.136 b 88.58 ± 3.240 a

D11: after 10 days of drought stress. D11R5: after 10 days of drought stress and 5 days of re-watering. CK: 75% ± 5% of field waterholding capacity; MS: 55% ± 5% of field waterholding capacity; SS: 35% ± 5% of field waterholding capacity. Different lowercase letters indicate significant differences between treatments (P < 0.05). Mean ± SE, n = 3.

capacity than maize and thus greater drought resistance [26]. In the present study, MS conditions did not reduce RL of sorghum and maize compared with CK (Table 1), suggesting that the stable Kr of sorghum under mild water stress may be attributed to a considerable accumulation of solutes. Our results also suggest that sorghum can endure moderate drought by adjusting certain plant traits, but is still as vulnerable as maize under severe drought stress.

Kr among species and treatments in our research were not restored to CK levels after re-watering (Table 1). The rate and extent of recovery from drought stress after re-watering are influenced by both the drought intensity and the drought tolerance of the species. Based on the indications provided by both drought-tolerant and drought-vulnerable plants used in our study, it is reasonable to propose that, at least under short-term drought stress, pre-drought conditions do not control the recovery rates of photosynthesis-related parameters, but could affect the recovery rates of Kr (Fig. 1 and Table 1). Kr can be influenced by external and internal factors such as water availability, soil conditions, embolisms in the xylem, and root traits [27]. Although root growth and favorable environments can increase Kr [28], the efficiency of repair of impaired hydraulic conductance and its related root characteristics differ considerably among species [29]. Our results showed that Kr, Ar, and RL of both treated sorghum and maize increased after re-watering but did not exceed the values of CK (Table 1). This finding suggests that the recovery abilities of Kr are similar between sorghum and maize, at least after a short time of re-watering, although the two species differ in drought tolerance.

Numerous factors affect drought recovery, including genotype, nutrient status, light, competition with other plants, plant phenology, plant size, intensity and/or duration of dehydration, and duration of re-hydration, and influence the physiological and morphological features of re-watered plants [30]. A recent study showed that some physiological traits, such as Gs, can be enhanced in drought-stressed plants after re-watering and that the values of these parameters often exceed those of controls [31], thus showing an overcompensation effect. In contrast, study have shown that after re-watering, the physiological traits of drought-treated plants do not recover to the levels of controls, reflecting pre-drought limitations [32]. The results of the present study showed that after rehydration, Pn, Gs, and Fv/Fm in treated sorghum recovered, but did not exceed the values of CK (Fig. 1). In contrast, Pn, Gs, and Fv/ Fm of maize under SS conditions exceeded those of CK and MS conditions at the late stage of rehydration (Fig. 1), showing overcompensation. It is well known that enhanced photosynthesis results in rapid plant growth, and our results confirmed this rule. After re-watering, Al and RL of sorghum experiencing SS conditions did not recover to CK level, owing to the slow recovery of photosynthesis (Fig. 1 and Table 1). In contrast, Al and RL of maize experiencing SS conditions recovered to CK level, accompanied by a rapid rise of photosynthesis (Fig. 1 and Table 1). Earlier stress activates the defense system against later stress by adjusting plant physiological process and morphological characteristics [33], a response that partly explains overcompensation as an adaptive response to recurring stress. Rapid growth as a response reaction to

environmental change, which results in overcompensation including rapid regrowth, has previously been discussed [34]. Rapid regrowth can occur after extreme conditions and has evolved as a strategy to minimize deleterious effects [35]. For pre-drought limitation, previous study also found that it may cause a residual memory, resulting in a plant growth pattern resembling that of a plant that has undergone drought stress [15], especially in plants without any damage to physiological functions. In the present study, pre-drought limitation occurred in the drought-tolerant plant species, but the drought-vulnerable plant species overcompensated. Thus, the degree of sensitivity to drought and the subsequent adjustment strategy play important roles in plant performance after rehydration. Although both pre-drought limitation and overcompensation are supported by empirical evidence, more data are needed to determine whether these two manifestations of plant behavior after rehydration can be clearly distinguished based on differing drought tolerance and on which phenomenon occurs after rehydration.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (No. 31500320) and the National Key Technology R&D Program of China (No. 2015BAD22B01).

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