Recovery period of long-term waterlogging exacerbates damage to photochemical phase of photosynthesis in bush beans (Phaseolus vulgaris L.).

doi:10.21203/rs.3.rs-3149450/v1

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Recovery period of long-term waterlogging exacerbates damage to photochemical phase of photosynthesis in bush beans (Phaseolus vulgaris L.).

https://doi.org/10.21203/rs.3.rs-3149450/v1

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Beans are considered one of the basic products of the farmer economy and food security. In some regions of the tropics, the presence of climatic phenomena involves the increase in the frequency and intensity of rainfall and causes different waterlogging periods. The objective of this work was to determine the effect of waterlogging duration and recovery on the growth and photosynthesis of bean plants. The experiment was carried out in the greenhouses, using a completely randomized design with four replicates per treatment. Bush bean plants that were subjected when they had 3-4 true leaves, to two periods of waterlogging, short-term (STW) and long-term (LTW), 7 and 14 days, respectively and 7 days of recovery period in both treatments, and one control in drainage condition. The STW caused a significant decrease in photosynthesis (P_n) (82%), stomatal conductance (g_s) (83%) and an increase in the content of malondialdehyde (MDA) and electrolyte leakage (EL) compared to control plants. In STW-RP, P_n, WUE, C_i/g_s ratio and photochemical quenching (qP) increased. Otherwise, the LWT reduced P_n (94%) and g_s (93%) compared to control plants. At the LTW-RP there was a reduction in the maximum photochemical efficiency of PSII (F_v/F_m), the content of chlorophyll and carotenoids and an increase in non-photochemical quenching (NPQ). Proline increase in LTW-RP was not enough to avoid damage to the PSII. The STW caused moderate stress on the photosynthesis of bean plants although plants can recover their photosynthetic activity in a low proportion. The LTW increases the damage of the photosynthetic apparatus, and its effect is exacerbated in the subsequent LTW-RP.

photosynthesis

malondialdehyde

abiotic stress

chlorophyll

hypoxia

The bean (Phaseolus vulgaris L.) is an important legume species as a worldwide crop (Karavidas et al. 2022), it belongs to the Fabaceae family and its center of origin is in Mesoamerica and South America, from Mexico to Argentina (Chacón S et al. 2005; Uebersax et al. 2022). Common bean is considered one of the most important sources of protein and nutrients for more than 300 million people in parts of Eastern Africa and Latin America (Karavidas et al. 2022). However, the yield bean crop is affected by water stress including both drought and waterlogging due to its sensitivity (Posso et al. 2020; Uebersax et al. 2022). In some tropic’s regions, climatic phenomena have intensified due to climate change and an increase in rainfall is expected (Horchani et al. 2010; Posso et al. 2020). The increase in the frequency and intensity of rainfall causes yield beans crops due to temporary waterlogging and oxygen deficiency (Sairam et al. 2009; Duran and Pinto 2011).

Waterlogging is an important abiotic stress that affects crop growth and production worldwide (Liu et al. 2020; Pandey et al. 2021). Waterlogging affects crops by inhibiting gaseous exchange between the roots and the atmosphere(Striker 2012; Striker and Colmer 2017) inducing physiological changes such as reduction in stomatal conductance, photosynthesis, and chlorophyll content (Velasco et al. 2019; Posso et al. 2020). In pigeon plants (Cajanus cajan L.) an increase in cell membrane damage has been reported when plants are subjected to waterlogging (Sairam et al. 2009). An increase in the activity of antioxidant enzymes has been reported in fava bean plants (Vicia faba L.) in the recovery period, after waterlogging (Pociecha 2013). It has also been observed that some plants have acclimation responses to waterlogging, such as the formation of adventitious roots that provide them with water, nutrients, and anchoring (Qi et al. 2020; Nuruzzaman Manik et al. 2022), as well as the formation of aerenchyma as a strategy for supplying O₂ from the shoots to the roots and to ventilate gasses such as CO₂ and methane in conditions of oxygen deficiency in the soil (Evans 2004; Kehoe et al. 2022; Geng et al. 2023). It has been reported that the effects of waterlogging on plants can be observed even long after the stress has ceased (Pociecha 2013; Posso et al. 2020). In bean plants, declines in chlorophyll a and b persist after the end of the waterlogging period (Pociecha et al. 2008). Similarly, short periods of waterlogging can have long-term effects on crop growth and yield (Kuai et al. 2015; Velasco et al. 2019). In part of South America, including Colombia, climatic phenomena such as La Niña produce an increase in the frequency and intensity of rainfall, causing periods of oxygen deficiency in the soil that can be short or prolonged (Duran and Pinto 2011; Velasco et al. 2019). Bean is planted on land with flat topography, favoring waterlogging of soils, which means that this crop is frequently subjected to periods of waterlogging of different durations (Gepts 1991; Collaku and Harrison 2002; Velasco et al. 2019; Posso et al. 2020). However, not much is known about the responses of shrub beans to waterlogging and few studies have been conducted to understand the recovery process after this stress (Pociecha 2013; Posso et al. 2020). We hypothesize that 'ICA Cerinza' bush beans may not tolerate prolonged waterlogging, and the recovery period after reoxygenation could exacerbate the damage caused by waterlogging stress. Therefore, the objectives of this study were (1) to investigate how the short-term waterlogging (STW) and long-term waterlogging (LTW) and the recovery period (RP) affects ICA Cerinza bush beans leaf gas exchange and chlorophyll fluorescence and (2) determinate the STW, LTW and RP affects growth parameters, leaf pigment content, electrolytes leakage and proline content of ICA Cerinza bush beans.

Plant material and growth conditions

The study was carried out in the greenhouses of the faculty of Agrarian Sciences of the National University of Colombia, Bogotá (4°35'56 " N and 74°04'51'' W). Cultivated 'ICA-Cerinza' bush beans were planted in pots of 1 L capacity, with soil and sand mixture (1: 1, v/v). The plants grew in a greenhouse with an average temperature of 22 ± 4°C, 40–90% RH and a photoperiod of 12h:12 hours day/darkness, respectively and the photosynthetically active radiation (PAR) at midday was 1500 µmol m^− 2 s^− 1. They were fertirrigated throughout the experiment once a week with full-strength Hoagland nutrient solution type (Hoagland and Arnon 1950).

Waterlogging and recovery treatments

The condition of oxygen deficiency in the substrate was established by covering the drainage holes of the pots to ensure a constant water depth of 2 cm above the surface of the substrate. The plants were exposed to two waterlogging periods, a short-term STW and long-term LTW, 7 and 14 days, respectively. The bean plants were subjected to the treatments when they presented three to four true leaves (around 14 days post-sowing). After each stress period, the plants were drained for 7 d until reaching approximately 80% of the pot capacity, considering this period as a recovery period (RP). In the control treatment, the soil moisture remained around 80% of pot capacity throughout the experiment (ISO 11465 1993). The experiment consisted of 64 plants in four replications (Fig. 1.)

Stem length

In each treatment the stem length was registered, from the stem base to the apical meristem, the data were recorded at the end of each waterlogging event and at the end of the recovery period. At the end of the trial, the number of adventitious roots per plant was determined by counting the lateral roots that were at least 2 mm long at the base of the stem.

Gas exchange and water-use efficiency

The rate of photosynthesis (P_n), the stomatal conductance (g_s), and the internal concentration of CO₂ (C_i) were measured on the second leaf from the top of the plant, between 9:00 am and 11:00 am with a CO₂ concentration of 400 µl L^− 1 and a photosynthetic photon flux density of 900 µmol m^− 2 s^− 1 using a portable system connected to an infrared gas analyzer (LI-6200, Lincoln, Nebraska, USA.). Transpiration (E) was determined using a steady state porometer (LI-1600, Lincoln, Nebraska, USA.). The water-use efficiency (WUE) was calculated as P_n/E ratio and expressed at µmol CO₂ / mmol H₂O.

Chlorophyll fluorescence parameters

To determine the presence of the PSII energy dissipation process, the maximum quantum yield (F_v/F_m) of photosystem II on dark adapted leaves was measured for 30 minutes using a MINI-PAM modulated fluorometer (Walz®, Effeltrich GmbH, Germany) (Yi et al. al., 2006). The measurement was made on the same leaves that were used to measure P_n. The chlorophyll molecules were excited for 60 seconds with 1500 µmol m^− 2 s^− 1 of actinic light. The variables of photosynthetic electron transport rate (ETR), real photochemical efficiency of PSII (Ф_PSII), photochemical extinction (qP), and non-photochemical extinction (NPQ) were recorded.

Leaf pigment content

Pigments were extracted in accordance with Sims and Gamon. (2002). For the extraction, 0.03 g of tissue from the second fully expanded leaf of four plants per treatment was homogenized in 80% acetone. The absorbance was determined at an optical density of 663 and 647 nm for chlorophyll and of 470 nm for carotenoids (Wellburn 1994).

Cell membrane stability

To estimate the stability of the cell membrane, the Malondialdehyde content (MDA) was determined as an indicator of the lipid peroxidation of the membranes, and electrolytes leakage (EL) was also quantified as an indicator of membrane permeability. The content of MDA was determined using the method of Hodges et al. (1999). Plant tissue samples were homogenized in alcohol:water in relation 80:20 (v:v) and centrifuged in 3000 g for 10 min. The samples were stirred and heated at 95°C for 25 min in a water bath, cooled and centrifuged at 3000 g for 10 min. Absorbance readings at 440, 532 and 660 nm were made using a spectrophotometer (Spectronic BioMate 3 UV-vis Thermo, Madison, WI, USA) and a molar extinction coefficient of 157 M mL^− 1 was used. were expressed as MDA equivalents (nmol g^− 1 FW). The leakage of electrolytes was determined by the method described by Gong et al. (1996) from 5 cm² of leaf tissue of the second leaf. Each sample was placed in a tube with 20 mL of deionized water and incubated at 30°C for 2h, after which the initial electrical conductivity of the medium (CE₁) was determined. Subsequently, each sample was boiled at 100°C in a water bath for 15 min and cooled, registering the final electrical conductivity (CE₂). The percentage of electrolytes was calculated with the formula: CE₁ / CE₂ × 100 [3]

Proline content

The level of proline was determined according to Bates et al. (1973) based on proline´s reaction with ninhydrin. For proline determination, a 1:1:1 solution of proline, ninhydrin, and glacial acetic was incubated at 100°C for 1 hour. The reaction was arrested in an iced bath, the chromophore was extracted with toluene and its absorbance was measured at 520 nm. The concentration of proline was determined using a standard curve and was expressed as µmol proline g^− 1 fresh weight (FW).

Statistical analysis

A one-way analysis of variance (ANOVA) was performed, data were tested for normal distribution using the Shapiro Wilk test; homoscedasticity was assessed using the Levene test, followed by a Tukey HSD test (p ≤ 0.05) to determine the effect of the treatments on the variables. The data was analyzed using the Statistix v 9.0 software (analytical software, Tallahassee, FL, US).

Growth parameters

The STW reduced the stem length by 41% (Fig. 2A), however, in STW-RP the plants reached the stem length of the non-waterlogged control treatment. The LTW reduced stem length by 14% and in LTW-RP no recovery was observed (Fig. 2B). In STW and LTW, there was formation of adventitious roots at the base of the stem, however, in the LTW they were significantly higher (Fig. 2C). Fig. 2D shows the beans plants visual changes in the control, STW and LTW treatments. STW beans plants show lost in the leaf turgor and LTW plants leaf chlorosis was more evident.

Gas exchange and water-use efficiency

STW treatment reduced P_n (82%), g_s (85%) and E (87%), and increased C_i (30%) (Fig. 3A-D). In the STW-RP only the P_n increased, (133%) (Fig. 3A). The LTW reduced P_n (94%), g_s (93%) and E (94%) and increased C_i (33%). During the LTW-RP, the values of P_n, g_s, E and C_i did not show differences with respect to LTW (Fig. 3E-H).

The bean plants in the STW-RP increased the WUE (8.62 μmol CO₂/mmol H₂O) with respect to control plants, while those at to the LTW-RP showed no variation in the WUE (Table 1). The relation C_i/C_a in STW (10%) and LTW (9%) increased with respect to the control plants. In the STW-RP, the C_i/C_a ratio decreased (4%) with respect to STW, while in the LTW-RP there was no variation. The C_i/g_s ratio increased in both STW and LTW, without significant differences with the RP (Table 1).

Chlorophyll fluorescence parameters

During STW plants presented a small but significant reduction in qP without significant differences in F_v/F_m, Ф_PSII, ETR, and NPQ (Table 2). Plants in LTW-RP showed only a reduction in F_v/F_m (0.73 ± 0.01), while Ф_PSII, ETR and qP decreased both in LTW and LTW-RP, but without presenting significant differences. The NPQ increased significantly (101%) during LTW and LTW-RP (246%) (Table 2).

Leaf pigment content

STW-RP plants showed a reduction in the Chl a (1.71 ± 0.33 mg g^-1 FW) and Total Chl (2.44 ± 0.41 mg g^-1 FW) content. The Chl a content decreased during the LTW (64%) and during LTW-RP (84%) with significant differences between them. The content of Chl b, Total Chl and Car only decreased during the LTW-RP (Table 3).

Cell membrane stability and proline content

In bean plants during the STW there was only a significant increase in electrolyte leakage and MDA content, while during the LTW-RP there was only an increase in proline content (Table 4).

Growth is one of the parameters most affected by the different types of stress, under waterlogging conditions, growth reduction has been reported in cotton (Gossypium hirsutum L.) (Kuai et al. 2015; Zhang et al. 2021b), tomato (Solanum lycopersicum L.) (Reid and Crozier 1971; Zhou et al. 2022), wheat (Triticum aestivum) (Huang et al. 2012; Ciancio et al. 2021), lulo (Solanum quitoense Lam) (Flórez-Velasco et al. 2015) and beans (Velasco et al. 2019)In this study, the waterlogging duration caused a reduction in growth like that reported for beans (Velasco et al. 2019; Posso et al. 2020). In cotton plants, different periods of waterlogging reduced growth in terms of plant height even after the end of the waterlogging (Kuai et al. 2015). In our study, the reduction in stem length was greater in the STW but increased in the STW-RP. The smallest decrease in stem length in the LTW could be due to an ethylene-mediated elongation response as observed in other plant species (Bailey-Serres and Voesenek 2008). The formation of adventitious roots has been considered a trait of acclimatization to waterlogging (Xu et al. 2022; Geng et al. 2023)and is reported in plants such as mung bean (Kumar et al. 2013), corn (Geng et al. 2023), wheat (Xu et al. 2022) and barley (Nuruzzaman Manik et al. 2022). Here, an increase in the number of adventitious roots was found in the STW and LTW, however, the adventitious roots do not exceed three mm in length (data not shown), which suggests that in bean plants need could be need more time to elongate adventitious roots or it have not energy to boost adventitious roots growth. They are probably not associated with tolerance in bush beans. The development of adventitious roots not associated with tolerance has been observed in tomato plants (S. lycopersicum L.) and is induced by the low availability of oxygen in the soil (Vidoz et al. 2010).

The effect of waterlogging on photosynthetic parameters in plants has been widely reported (Kumar et al. 2013; Najeeb et al. 2015; Pan et al. 2021). Our results show during the waterlogging and recovery the reduction in P_n and g_s, which suggests that the decrease in P_n may be due in part to a stomatal limitation. The waterlogging induces cytoplasmic acidification and protonation of aquaporins, affecting the water intake and the hydraulic conductivity of the root, causing stomatal closure(Tournaire-Roux et al. 2003). On the other hand, the increase in C_i found here suggests the decrease in P_n may also be associated with the presence of non-stomatal limitations (Farquhar and Sharkey 2003; Sun et al. 2013; Olorunwa et al. 2022).

During the STW-RP, only an increase in P_n was observed while g_s, E and C_i did not show variations indicating that this period of waterlogging produces a stress that allows the plant to recover its photosynthetic activity although in a low proportion. Ahmed et al. (2002) found increases in P_n in plants of mung beans (Vigna radiata L.) subjected to 8 days of waterlogging and recovery. Likewise, in this study during the STW-RP, WUE increased, indicating that E decreased more than P_n. According to Pezeshki (2001), low g_s can maintain the plant water balance by reducing water losses through transpiration. It has been reported that plants that have high rates of P_n and WUE may have higher growth and yield potential under fluctuating environmental conditions (Jones 1993). In this way, our results suggest that ICA-Cerinza bean plants subjected to the STW have a greater potential for growth and yield than those subjected to the LTW. Sheshshayee et al. (1996) reported the C_i/g_s ratio as an indicator of mesophyll efficiency. In this study, an increase in C_i/g_s values was found in both periods of waterlogging and recovery, which indicates a reduction in mesophyll efficiency. A high relation between the relation C_i/g_s and the content and efficiency of the Rubisco has been reported (Sheshshayee et al. 1996). In plants of clover (Trifolium pratense L.), tomato (S. lycopersicum L.) and cowpea (Olorunwa et al. 2022) has been reported a reduction in Rubisco levels due to waterlogging (Ahsan et al. 2007; Stoychev et al. 2013). These reports, together with the increase in C_i observed in this study, support that the reduction in photosynthesis is also due to non-stomatal limitations.

Decline in F_v/F_m have been associated with damage to PSII and have been observed in many plants under stress conditions (Zhao et al. 2014; Lin et al. 2022). Here, it was observed possible damage in PSII due to F_v/F_m decline in the LTW-RP. In addition, Ф_PSII, ETR and qP were similarly reduced, suggesting an effect of waterlogging on the efficiency of the photosynthetic apparatus in LTW and LTW-RP. Likewise, there was an increase in NPQ that may be associated with photoprotection mechanisms such as the xanthophyll cycle (Adams et al. 1995; Zhang et al. 2021a). These results are different from that reported by Smethurst et al. 2005 who found, in alfalfa plants (Medicago sativa L.), a complete recovery of the fluorescence parameters of chlorophyll in the drainage period, after 20 days of waterlogging. During STW, a reduction in qP was observed and during STW-RP an increase in qP that is consistent with the increase in P_n was observed.

A decrease in the chlorophyll content as a common symptom in plants subjected to waterlogging (Rao and Li 2003; Yu et al. 2019). Here, only a reduction in Chl a and Chl Total content during the STW-RP was observed, while in the LTW and LTW-RP had a reduction in the Chl content. Likewise, during the LTW-RP there was a decrease in Chl b and Car indicating a greater degradation. Similar data have been reported in bean plants (V. faba L.), where waterlogging caused a decrease in the Chl a content and that remained during the recovery period (Pociecha 2013). It is known that waterlogging induces the synthesis of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) that is transported to the aerial part of the plant and converted into ethylene, a hormone that induces the activation of enzymes that degrade chlorophylls (Christianson et al. 2010; Sharma et al. 2022). Likewise, the reduction of chlorophylls can also be a mechanism of photoprotection under stress conditions, since it reduces the number of photons absorbed by the leaves (Galmés et al. 2007). The reduction in the chlorophyll and carotenoid content observed in this study may be associated with the reduction in F_v/F_m (Shangguan et al. 2000; Sharma et al. 2022).

The stability of the cell membrane in plants is directly related to the functioning of cellular metabolism and under stress conditions, it is highly affected by the presence of reactive oxygen species (ROS) (Silva et al. 2020; Mittler et al. 2022). Under waterlogging conditions, an increase in ROS has been found due to the production of O₂- dependent on NADPH oxidase (Qi et al. 2019). Likewise, lipid peroxidation changes the permeability of the membrane, so electrolyte leakage is a measure of the integrity of the membrane (Zhang et al. 2019). Here we found an increase in MDA content and electrolyte leakage only in the STW, Bansal and Srivastava (2015) found in pigeon plant (Cajanus cajan L. Mill) subjected to six days of waterlogged increase in damage to the cell membrane. During the LTW the MDA content and electrolyte leakage did not vary with respect to control plants suggesting the presence of a defense response at the level of production of antioxidants or protective molecules of the membranes. Pociecha (2013) reported increases in the activity of enzymes Peroxidases and Ascorbate peroxidase in bean plants (V. faba L.) subjected to waterlogging and 7 days of recovery. The increase in the synthesis of the proline has been reported in response to different abiotic stresses where it is attributed a role as osmolyte and antioxidant (Hamilton and Heckathorn 2001; Claussen 2005; Barickman et al. 2019). The accumulation of proline observed here during LTW, and LTW-RP may explain in part that no damage to the stability of the membrane has occurred in the LTW as suggested by the MDA content and electrolyte leakage data. However, the F_v/F_m was lower in these plants, may be the concentration of proline produced is not sufficient to prevent PSII damage in bush beans plants. Otherwise, plants of Capsicum sp dramatically increase the proline content when subjected to waterlogging conditions, which confers a slight resistance to waterlogging (Ou et al. 2011).

In conclusion, waterlogging can have a negative impact on the growth and photosynthesis of bush bean plants, with the severity of the effect depending on the duration of the waterlogging period. STW can cause moderate stress while LTW can significantly reduce photosynthetic activity and cause damage to the photosynthetic apparatus. However, some recovery of photosynthetic activity can occur during the STW-RP and in the LTW-RP the damage in the photosynthetic apparatus is exacerbated whit concomitant reduction in growth. This information can be useful for farmers and researchers in finding ways to mitigate the negative effects of waterlogging on bean crops, which are important for food security in many regions of world.

Author Contributions: Nixon Florez was involved in conceptualization, investigation data acquisitions, statistics analysis, and writing—review and editing; Gustavo Ligarreto resources, and project administration; Hermann Restrepo, supervision and project administration; Liz Patricia, investigation, writing—original draft preparation, funding acquisitions and writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Conflicts of Interest: The authors declare no conflict of interest.

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Table 1. Effect of short-term waterlogging (STW) and long-term waterlogging (LTW) and recovery period (RP) on water-use efficiency (WUE), C_i/C_a ratio and mesophyll efficiency (C_i/g_s) in leaves shrub bean plants.

Treatments	WUE (µmol m-2 s-1/mmol m-2 s-1)	Ci/Ca	Ci/gs
	STW
Control	2.12^z ± 0.08 b^y	0.88 ± 0.00 c	0.88 ± 0.04 b
STW	3.40 ± 0.47 ab	0.97 ± 0.00 a	5.09 ± 0.62 a
STW-RP	8.62 ± 2.42 a	0.93 ± 0.01 b	6.45 ± 1.62 a
	LTW
Control	2.28 ± 0.33 a	0.89 ± 0.01 b	0.82 ± 0.02 b
LTW	2.30 ± 0.93 a	0.97 ± 0.01 a	13.19 ± 1.21 a
LTW-RP	3.05 ± 0.95 a	0.94 ± 0.02 ab	11.26 ± 0.94 a

^Z Values are means of 4 replicates ± S. E.

^Y Means with different letters represent statistically significant differences according to Tukey's test (p≤0.05).

Table 2. Effect of short-term waterlogging (STW) and long-term waterlogging (LTW) and recovery period (RP) on maximal efficiency of PSII photochemistry (F_v/F_m) in dark-adapted leaves, actual photochemical efficiency of PSII (Ф_PSII), non-photochemical quenching (NPQ), electron transport rate of PSII (ETR), photochemical quenching (qP) in leaves of shrub bean plants.

Treatments	F_v/F_m	ɸPSII	ETR (µmol m-2 s-1)	qP	NPQ
	STW
Control	0.8^z ± 0.00 a^y	0.45 ± 0.04 a	283.97 ± 26.51 a	0.67 ± 0.04 a	1.03 ± 0.20 a
STW	0.78 ± 0.00 a	0.32 ± 0.04 a	200.97 ± 26.33 a	0.46 ± 0.02 b	1.21 ± 0.17 a
STW-RP	0.8 ± 0.01 a	0.45 ± 0.03 a	220.50 ± 29.58 a	0.7 ± 0.04 a	1.17 ± 0.19 a
	LTW
Control	0.79 ± 0.00 a	0.53 ± 0.01 a	334.69 ± 8.61 a	0.74 ± 0.01 a	0.64 ± 0.06 c
LTW	0.79 ± 0.00 a	0.35 ± 0.05 b	285.23 ± 20.12 b	0.61 ± 0.04 b	1.29 ± 0.11 b
LTW-RP	0.73 ± 0.01 b	0.24 ± 0.01 b	150.57 ± 9.18 b	0.50 ± 0.02 b	2.22 ± 0.09 a

^Z Values are means of 4 replicates ± S. E.

^Y Means with different letters represent statistically significant differences according to Tukey's test (p≤0.05).

Table 3. Effect of short-term waterlogging (STW) and long-term waterlogging (LTW) and recovery period (RP) chlorophyll (Chl) a, b and Total, and Carotenoid (Car) contents in leaves shrub bean plants.

Treatments	Chl a (mg g^-1 FW)	Chl b (mg g^-1 FW)	Total Chls (mg g^-1 FW)	Car (mg g^-1 FW)
	STW
Control	4.43^z ± 0.62a^y	1.13 ± 0.30a	5.56 ± 0.92a	0.42 ± 0.02 a
STW	3.80 ± 0.41a	1.11 ± 0.32a	4.92 ± 0.71ab	0.45 ± 0.02 a
STW-RP	1.71 ± 0.33b	0.72 ± 0.10a	2.44 ± 0.41b	0.37 ± 0.02 a
	LTW
Control	4.22 ± 0.71a	1.42 ± 0.2a	5.64 ± 1.51a	0.41 ± 0.01a
LTW	1.93 ± 0.40b	0.24 ± 0.2a	2.20 ± 0.5a	0.37 ± 0.02a
LTW-RP	0.64 ± 0.42c	0.16 ± 0.2b	0.76 ± 0.6b	0.25 ± 0.01b

^Z Values are means of 4 replicates ± S. E.

^Y Means with different letters represent statistically significant differences according to Tukey's test (p≤0.05).

Table 4. Effect of short-term waterlogging (STW) and long-term waterlogging (LTW) and recovery period (RP) on electrolytes leakage, Malondialdehyde (MDA) and Proline contents in shrub bean plants.

Treatments	Electrolytes leakage (%)	MDA (µmol g^-1 FW)	Proline (µmol g^-1FW)
	STW
Control	14.8^z ± 1.17 b^y	4.06 ± 0.92 b	29.22 ± 6.59 a
STW	21.17 ± 1.42 a	13.65 ± 1.08 a	22.89 ± 5.89 a
STW-RP	18.51 ± 1.33 ab	3.52 ± 0.62 b	25.4 ± 4.04 a
	LTW
Control	15.71 ± 0.48 a	5.44 ± 0.78 a	29.43 ± 2.13 b
LTW	18.99 ± 2.05 a	3.8 ± 0.33 a	41.24 ± 2.67 ab
LTW-RP	20.21 ± 1.18 a	4.49 ± 0.57 a	52.85 ± 4.35 a

^Z Values are means of 4 replicates ± S. E.

^Y Means with different letters represent statistically significant differences according to Tukey's test (p≤0.05).

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Recovery period of long-term waterlogging exacerbates damage to photochemical phase of photosynthesis in bush beans (Phaseolus vulgaris L.).

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Abstract

Figures

Introduction

Materials and Methods

Plant material and growth conditions

Waterlogging and recovery treatments

Stem length

Gas exchange and water-use efficiency

Chlorophyll fluorescence parameters

Leaf pigment content

Cell membrane stability

Proline content

Statistical analysis

Results

Discussion

Conclusions

Declarations

References

Tables

Status:

Version 1