The Effect of Waterlogging at the Vegetative Stage on Shoot and Root Growth of Chickpea Cultivars (Cicer arietinum L.)

Document Type : Original Article

Authors

• Leila Siahkamary
• Mohammad Eghbal Ghobadi
• Mokhtar Ghobadi
• Saeid Jalali Honarmand

Department of Plant Production and Genetics, Faculty of Agricultural Science and Engineering, Razi University, Kermanshah, Iran

10.22067/ijpr.2024.84854.1069

Abstract

Introduction
Chickpea (Cicer arietinum L.) is a plant from the legume family, which is usually cultivated under rainfed conditions. This crop is mostly cultivated in late winter or early spring. In these conditions, there is a high probability of heavy rains (short or long term) and there is a possibility of waterlogging in early spring and during the early growing stages of chickpea. In waterlogged conditions, due to the lack or absence of oxygen in the plant roots occur anaerobic conditions and greatly reduced the amount of energy production in the roots. In this case, the root does not have the necessary energy to transport materials from the cell membrane, and plants face ionic stress, reduced hydraulic conductivity, and reduced water absorption. Reduced and disrupted root growth leads to diminished shoot growth, impaired water and nutrient absorption, and ultimately lower grain yield. In general, the extent of damage caused by oxygen deficiency depends on the plant species, variety, growth stage, soil type, and environmental conditions. Therefore, the purpose of this experiment was to investigate the effects of waterlogging on chickpea cultivars (Desi and Kabuli), physiological characteristics, root growth and yield.
 
Materials and Methods
This experiment was carried out as factorial based on completely randomized design (CRD) in three replications in the research farm via pot of the Campus of Agriculture and Natural Resources, Razi University, Kermanshah, Iran in 2013-2014. Factors included chickpea cultivars ILC482 and Azad (from Kabuli type) and Kaka and Pirooz (from Desi type) and duration of waterlogging including no waterlogging (control), 4, 8 and 12 days at 30 days after planting (vegetative stage). Physiological traits (relative water content, membrane stability and pigments) as well as total root length, root dry weight, number of nodes, main root length and root volume in a destructive way in the pod setting stage, as well as in the ripening stage, root traits, remobilization, relative water content, membrane stability, pigments, seed protein, biological yield, seed yield, 100-seed weight and plant height were investigated. Planting was done in the first year on March 11, 2013 and in the second year on March 15, 2014. The size of plastic pots was 30 x 30 cm. 30 days after planting were applied treatments. Compound analysis of data was done with SAS software and means comparisons were performed using the least significant difference (LSD) at the 5% level.
 
Results and Discussion
The results of compound analysis showed that there were significant differences between the two years in seed yield and the number of seeds per plant. In the second year, the seed yield and the number of seeds per plant compared to the first year increased by 16.9% and 12.1%, respectively. In the second year, the ambient temperature was lower. At a lower temperature, the waterlogging damage is more severe to plants. The total dry matter yield of chickpea cultivars in waterlogged conditions was significantly different and Kaka, Pirooz, ILC482 and Azad cultivars were 4.42, 3.19, 2.99 and 2.54 g.plant^-1, respectively. The highest damage to seed yield in waterlogging in 12 days was related to Azad variety (71% compared to the control). In waterlogged conditions, the seed yield was in Kaka (1.51 g.plant^-1), Pirooz (1.16 g.plant^-1), ILC482 (0.95 g.plant^-1) and Azad (0.97 g.plant^-1). There was a significant difference between Kabuli type and Desi type, however, grain yield in Desi type was 28.3% higher than Kabuli type. In the pod setting stage, the Pirooz cultivar in the control treatment had the highest total root length with 7741 cm (in the first year) and 7432 cm (in the second year), but the lowest was in the second year at the Kaka cultivar and 12 days with 440 cm. In general, with the increase of the duration of flooding in chickpea cultivars, the total root length decreased significantly and between 4 days, 48.4 to 60.4 percent, 8 days to 8.8 to 70.8 percent, and 1.12 days from 81 to 89.4 percent. In all treatments, the control treatment (without waterlogging) had the highest chlorophyll a, and the amount of chlorophyll a decreased in other treatments. However, no reduction was observed in Pirooz in 4, 8 and 12-day treatment. Chlorophyll b had a different response to waterlogging levels and cultivar. Chlorophyll b was the highest in ILC482 in control treatment, while in Azad, Kaka and Pirooz treatments, chlorophyll b increased with increasing duration of waterlogging. Pigment carotenoids in ILC482 and Azad significantly decreased with increasing duration of waterlogging, but it was not significant in Kaka and Pirooz cultivars. Overall, carotenoids were less fluctuating in the desi type.
 
Conclusions
Waterlogging in the vegetative stage even for 4 days with a decreasing effect on total root length, number of nitrogen fixing nodes, plant height, total dry matter, chlorophyll and carotenoids content, membrane stability index, relative leaf water content, biological yield, seed protein, the number of seeds per plant and the weight of 100 seeds and finally caused a decrease in seed yield. Among the components of seed yield, the amount of damage was higher on the number of seeds per plant. In general, the seed yield of ILC482 and Azad (Kabuli type) was lower than that of Kaka and Pirooz (Desi type). In the second year, due to the lower air temperature compared to the first year, the damage to the total root length and total dry matter decreased. This experiment provides valuable results on the response mechanisms of chickpea to waterlogging stress and can help develop strategies to improve its performance in waterlogged environments, which are expected to waterlogging increase due to climate change. However, more research is needed to investigate the response of different chickpea species to short-term and long-term waterlogging conditions.

Keywords

• Photosynthetic pigments
• Leaf relative water content
• Remobilization
• Total root length

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©2024 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0).

References

Adegoye, G. A., Olorunwa, O. J., Alsajri, F. A., Walne, C. H., Wijewandana, C., Kethireddy, S. R., ... & Reddy, K. R. (2023). Waterlogging effects on soybean physiology and hyperspectral reflectance during the reproductive stage. Agriculture, 13(4), 844. https://doi.org/10.3390/agriculture13040844

Anee, T. I., Nahar, K., Rahman, A., Mahmud, J. A., Bhuiyan, T. F., Alam, M. U., Fujita, M., & Hasanuzzaman, M. (2019). Oxidative damage and antioxidant defense in Sesamum indicum after different waterlogging durations. Plants, 8, 196. https://doi.org/10.3390/plants8070196

AOAC. (1990). Association of official analytical chemists. 15^th Ed., Method No: 988.05, p. 70.

Arndt, S. K., Irawan, A., & Sanders, G. J. (2015). Apoplastic water fraction and rehydration techniques introduce significant errors in measurements of relative water content and osmotic potential in plant leaves. Physiologia Plantarum, 155, 355-368. https://doi.10.1111/ppl.12380

Ashraf, M. A. (2012). Waterlogging stress in plants: A review. African Journal of Agricultural Research, 7(13), 1976-1981. https://doi.10.5897/AJARX11.084

Bailey‐Serres, J., & Colmer, T. D. (2014). Plant tolerance of flooding stress–recent advances. Plant, Cell and Environment, 37, 2211-2215. https://doi.10.1111/pce.12420

Bansal, R., & Srivastava, J. (2015). Effect of waterlogging on photosynthetic and biochemical parameters in pigeon pea. Russian Journal of Plant Physiology 62, 322-327. https://doi.10.1134/S1021443715030036

Barrs, H., & Weatherley, P. (1962). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences, 15, 413-428. http://dx.doi.org/10.1071/BI9620413

Chugh, V., Kaur, N., Gupta, A. K., & Rai, A. (2022). The seed biochemical signature as a potent marker for waterlogging tolerance in maize. Plant Stress, 4, 100085. https://doi.org/10.1016/j.stress.2022.100085

Dalai, D., & Sardar, S. S. (2021). Tolerance response of sunflower (Helianthus annuus L.) cultivar NSSH-1084 to waterlogging stress. International Journal of Current Microbiology and Applied Sciences, 10, 219-233. https://doi.org/10.20546/ijcmas.2021.1008.026

Daniel, K., & Hartman, S. (2023). How plant roots respond to waterlogging. Journal of Experimental Botany Erad, 332. https://doi.org/10.1093/jxb/erad332

Di Bella, C. E., Grimoldi, A. A., Lopardo, M. S. R., Escaray, F. J., Ploschuk, E. L., & Striker, G. G. (2016). Differential growth of Spartina densiflora populations under saline flooding is related to adventitious root formation and innate root ion regulation. Functional Plant Biology, 43, 52-61. http://dx.doi.org/10.1071/fp15149

Enkhbat, G., Ryan, M. H., Nichols, P. G., Foster, K. J., Inukai, Y., & Erskine, W. (2022). Petiole length reduction is an indicator of waterlogging stress for Trifolium subterraneum ssp. yanninicum. Plant and Soil, 475, 645-667. https://doi.org/10.1007/s11104-022-05404-6

Gedam, P. A., Shirsat, D. V., Arunachalam, T., Ghosh, S., Gawande, S. J., Mahajan, V., Gupta, A. J. & Singh, M. (2022). Screening of onion (Allium cepa L.) genotypes for waterlogging tolerance. Frontiers in Plant Science, 12, 727262. https://doi.10.3389/fpls.2021.727262

Ghobadi, M. E., Ghobadi, M., & Zebarjadi, A. (2017). Effect of waterlogging at different growth stages on some morphological traits of wheat varieties. International Journal of Biometeorology, 61, 635-645. https://doi.org/10.1007/s00484-016-1240-x

Habibullah, M., Sarkar, S., Islam, M. M., Ahmed, K. U., Rahman, M. Z., Awad, M. F., ElSayed, A. I., Mansour, E., & Hossain, M. S. (2021). Assessing the response of diverse sesame genotypes to waterlogging durations at different plant growth stages. Plants, 10, 2294. https://doi.org/10.3390/plants10112294

Hasani, S., Galeshi, S., Zeinali, E., Torabi, B., & Khadempir, M. (2019). Evaluation of tolerance and resistance to flooding stress in different soybean varieties. Environmental Stresses in Crop Sciences, 12, 1323-1313. https://doi.org/10.22077/escs.2019.1651.1369

Huang, X., Shabala, S., Shabala, L., Rengel, Z., Wu, X., Zhang, G., & Zhou, M. (2015). Linking waterlogging tolerance with Mn²⁺ toxicity: A case study for barley. Plant Biology, 17, 26-33. https://doi.10.1111/plb.12188

Jurczyk, B., Pociecha, E., Kościelniak, J., & Rapacz, M. (2016). Different photosynthetic acclimation mechanisms are activated under waterlogging in two contrasting Lolium perenne genotypes. Functional Plant Biology, 43, 931-938. http://dx.doi.org/10.1071/fp15339

Kaur, G., Singh, G., Motavalli, P. P., Nelson, K. A., Orlowski, J. M., & Golden, B. R. (2020). Impacts and management strategies for crop production in waterlogged or flooded soils: A review. Agronomy Journal, 112, 1475-1501. https://doi.org/10.1002/agj2.20093

Krishnamurthy, L., Upadhyaya, H., Saxena, K., & Vadez, V. (2012). Variation for temporary waterlogging response within the mini core pigeonpea germplasm. The Journal of Agricultural Science, 150, 357-364. https://doi.org/10.1017/S0021859611000682

Kuai, J., Liu, Z., Wang, Y., Meng, Y., Chen, B., Zhao, W., Zhou, Z., & Oosterhuis, D. M. (2014). Waterlogging during flowering and boll forming stages affects sucrose metabolism in the leaves subtending the cotton boll and its relationship with boll weight. Plant Science, 223, 79-98. http://dx.doi.org/10.1016/j.plantsci.2014.03.010

Kumar, P., Pal, M., Joshi, R., & Sairam, R. (2013). Yield, growth and physiological responses of mung bean [Vigna radiata (L.) Wilczek] genotypes to waterlogging at vegetative stage. Physiology and Molecular Biology of Plants, 19, 209-220. https://doi.10.1007/s12298-012-0153-3

Kyu, K. L., Malik, A. I., Colmer, T. D., Siddique, K. H., & Erskine, W. (2021). Response of mungbean (cvs. Celera II-AU and Jade-AU) and blackgram (cv. Onyx-AU) to transient waterlogging. Frontiers in Plant Science, 12, 709102. https://doi.org/10.3389/fpls.2021.709102

Li, C., Jiang, D., Wollenweber, B., Li, Y., Dai, T., & Cao, W. (2011). Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat. Plant Science, 180, 672-678. http://dx.doi.org/10.1016/j. plantsci.2011.01.009

Liu, R., Yang, C., Zhang, G., Zhang, L., Yang, F., & Guo, W. (2015). Root recovery development and activity of cotton plants after waterlogging. Agronomy Journal, 107, 2038-2046. https://doi.10.2134/agronj14.0567

Loreti, E., van Veen, H., & Perata, P. (2016). Plant responses to flooding stress. Current Opinion in Plant Biology, 33, 64-71. https://doi.org/10.1016/j.pbi.2016.06.005

Manik, S., Pengilley, G., Dean, G., Field, B., Shabala, S., & Zhou, M. (2019). Soil and crop management practices to minimize the impact of waterlogging on crop productivity. Frontiers in Plant Science, 140. https://doi.org/10.3389/fpls.2019.00140

Mano, Y., & Oyanagi, A. (2009). Trends of waterlogging tolerance studies in the Poaceae. Japanese Journal of Crop Science, 78, 441-448. https://doi.10.1626/jcs.78.441

Marti, J., Savin R., & Slafer, G. (2015). Wheat yield as affected by length of exposure to waterlogging during stem elongation. Journal of Agronomy and Crop Science, 201, 473-486. https://doi.10.1111/jac.12118

Mutava, R. N., Prince, S. J. K., Syed, N. H., Song, L., Valliyodan, B., Chen, W., & Nguyen, H. T. (2015). Understanding abiotic stress tolerance mechanisms in soybean: A comparative evaluation of soybean response to drought and flooding stress. Plant Physiology and Biochemistry, 86, 109-120. https://dx.doi.org/10.1016/j.plaphy.2014.11.010

Oh, M., & Komatsu, S. (2015). Characterization of proteins in soybean roots under flooding and drought stresses. Journal of Proteomics, 114, 161-181. https://doi.org/10.1016/j.jprot.2014.11.008

Olorunwa, O. J., Adhikari, B., Brazel, S., Bheemanahalli, R., Barickman, T. C., & Reddy, K. R. (2023). Waterlogging stress reduces cowpea (Vigna unguiculata L.) genotypes growth, seed yield, and quality at different growth stages: Implications for developing tolerant cultivars under field conditions. Agricultural Water Management, 284, 108336. https://doi.org/10.1016/j.agwat.2023.108336

Olorunwa, O. J., Adhikari, B., Shi, A., & Barickman, T. C. (2022). Screening of cowpea (Vigna unguiculata (L.) Walp.) genotypes for waterlogging tolerance using morpho-physiological traits at early growth stage. Plant Science, 315, 111136. https://doi.org/10.1016/j.plantsci.2021.111136

Palta, J., Ganjeali, A., Turner, N., & Siddique, K. (2010). Effects of transient subsurface waterlogging on root growth, plant biomass and yield of chickpea. Agricultural Water Management, 97, 1469-1476. http://dx.doi.org/10. 1016/j.agwat. 2010.05.001

Papakosta, D. K., & Gagianas, A. (1991). Nitrogen and dry matter accumulation, remobilization, and losses for Mediterranean wheat during grain filling. Agronomy Journal, 83, 864-870. http://doi.10.2134/agronj1991.00021962008300050018x

Pociecha, E. 2013. Different physiological reactions at vegetative and generative stage of development of field bean plants exposed to flooding and undergoing recovery. Journal of Agronomy and Crop Science, 199, 195-199. https://doi.org/10.1111/jac.12009

Rahman, M. N., & Shozib, S. H. (2021). Seasonal variability of waterlogging in Rangpur city corporation using GIS and remote sensing techniques. Geosfera Indonesia, 6, 143-156. https://doi.org/10.19184/geosi.v6i2.21006

Rajendran, A., Lal, S. K., Raju, D., Mallikarjun, B. P., Ramlal, A., & Sharma, D. (2023). Waterlogging tolerance evaluation methods for soybean (Glycine max (L.) Merr.) at the pregermination stage. Genetic Resources and Crop Evolution, 70, 2451-2461. https://doi.org/10.1007/s10722-023-01573-0

Rane, J., Singh, A. K., Kumar, M., Boraiah, K. M., Meena, K. K., Pradhan, A., & Prasad, P. V. (2021). The adaptation and tolerance of major cereals and legumes to important abiotic stresses. International Journal of Molecular Sciences, 22, 12970. https://doi.org/10.3390/ijms222312970

Ren, B., Zhang, J., Dong, S., Liu, P., & Zhao, B. (2016). Effects of duration of waterlogging at different growth stages on grain growth of summer maize (Zea mays L.) under field conditions. Journal of Agronomy and Crop Science, 202, 564-575. https://doi.10.1111/jac.12183

Richardson, A. D., Duigan, S. P., & Berlyn, G. P. (2002). An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytologist, 153, 185-194. https://doi.10.1046/j.0028-646X.2001.00289.x

Sairam, R. K., Rao, K. V., & Srivastava, G. (2002). Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Science, 163, 1037-1046. http://dx.doi.org/10.1016/S0168-9452(02)00278-9

Sasidharan, R., & Voesenek, L. A. (2015). Ethylene-mediated acclimations to flooding stress. Plant Physiology, 169, 3-12. https://dx.doi.org/10.1104/pp.15.00387

Sauter, M. (2013). Root responses to flooding. Current Opinion in Plant Biology, 16, 282-286. http://dx.doi.org/ 10.1016/j.pbi.2013.03.013

Shabala, S., Shabala, L., Barcelo, J., & Poschenrieder, C. (2014). Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant, Cell and Environment, 37, 2216-2233. https://doi.10.1111/pce.12339

Sharma, S., Bhatt, U., Sharma, J., Kalaji, H., Mojski, J., & Soni, V. (2022). Ultrastructure, adaptability, and alleviation mechanisms of photosynthetic apparatus in plants under waterlogging: A review. Photosynthetica, 60, 430-444. https://doi.10.32615/ps.2022.033

Singh, A. (2017). Waterlogging and salinity management for sustainable irrigated agriculture. I: Overview, implication, and plant response. Journal of Irrigation and Drainage Engineering, 143, 04017035. https://doi.org/10.1061/(ASCE)IR.1943-4774.0001226

Solaiman, Z., Colmer, T., Loss, S., Thomson, B., & Siddique, K. (2007). Growth responses of cool-season grain legumes to transient waterlogging. Australian Journal of Agricultural Research, 58, 406-412. https://doi.org/10.1071/AR06330

Sullivan, M., VanToai, T., Fausey, N., Beuerlein, J., Parkinson, R., & Soboyejo, A. (2001). Evaluating on-farm flooding impacts on soybean. Crop Science, 41, 93-100. https://doi.10.2135/cropsci2001.41193x

Tennant, D. (1975). A test of a modified line intersects method of estimating root length. Journal of Ecology, 63(3), 995-1001. https://doi.10.2307/2258617

Tiryakioglu, M., Karanlik, S., & Arslan, M. (2015). Response of bread-wheat seedlings to waterlogging stress. Turkish Journal of Agriculture and Forestry, 39, 807-816. https://doi.10.3906/tar-1407-124

Valliyodan, B., Ye, H., Song, L., Murphy, M., Shannon, J. G., & Nguyen, H. T. (2017). Genetic diversity and genomic strategies for improving drought and waterlogging tolerance in soybeans. Journal of Experimental Botany, 68, 1835-1849. https://doi.org/10.1093/jxb/erw433

Wiraguna, E., Malik, A. I., & Erskine, W. (2017). Waterlogging tolerance in lentil (Lens culinaris Medik. subsp. culinaris) germplasm associated with geographic origin. Genetic Resources and Crop Evolution, 64(3), 579-586. https://doi.10.1007/s10722-016-0385-0

Wu, X., Tang, Y., Li, C., Wu, C., & Huang, G. (2015). Chlorophyll fluorescence and yield responses of winter wheat to waterlogging at different growth stages. Plant Production Science, 18, 284-294. http://dx.doi.org/10.1626/pps.18.284

Yiu, J. C., Liu, C. W., Kuo, C. T., Tseng, M. J., Lai, Y. S., & Lai, W. J. (2008). Changes in antioxidant properties and their relationship to paclobutrazol‐induced flooding tolerance in Welsh onion. Journal of the Science of Food and Agriculture, 88, 1222-1230. https://doi.10.1002/jsfa.3209

Zahra, N., Hafeez, M. B., Shaukat, K., Wahid, A., Hussain, S., Naseer, R., Raza, A., Iqbal, S., & Farooq, M. (2021). Hypoxia and anoxia stress: Plant responses and tolerance mechanisms. Journal of Agronomy and Crop Science, 207, 249-284. https://doi.org/10.1111/jac.12471

Zhang, X., Jiang, D., Zheng, C., Dai, T., & Cao, W. (2011). Post‐anthesis salt and combination of salt and waterlogging affect distributions of sugars, amino acids, Na⁺ and K⁺ in wheat. Journal of Agronomy and Crop Science, 197, 31-39. https://doi.10.1111/j.1439-037X.2010.00438.x

Zhou, W., Chen, F., Meng, Y., Chandrasekaran, U., Luo, X., Yang, W., & Shu, K. (2020). Plant waterlogging/flooding stress responses: From seed germination to maturation. Plant Physiology and Biochemistry, 148, 228-236. https://doi.org/10.1016/j.plaphy.2020.01.020

Zhu, M., Li, F., & Shi, Z. (2016). Morphological and photosynthetic response of waxy corn inbred line to waterlogging. Photosynthetica, 54, 636-640. https://doi.10.1007/s11099-016-0203-0