Genotypic variation in response to drought stress is associated with biochemical and transcriptional regulation of ureides metabolism in common bean (Phaseolus vulgaris L.)

Motlalepula PHOLO-TAIT, Thuto KGETSE, Gaone Nthabeleng TSHEKO, Olerato Tshotlhe THEDI, Katso LETHOLA, Ebenezer Oteng MOTLAMME, Moagisi Innocent ITHUTENG, Samodimo NGWAKO

Abstract


Ureidic legumes such as common bean (Phaseoulus valgaris L.) plants export nitrogen from the nodules to shoots and leaves as ureides during symbiotic biological nitrogen fixation. Common bean gene encoding allantoinase (allantoin amidohydrolase, EC 3.5.2.5), is a key enzyme that catalyses the hydrolysis of allantoin to allantoic acid. It plays a role in ureide generation for export and ureide catabolism to generate a nitrogen source in sinks tissues. As such, one of the adaptive mechanisms of plants to drought stress, is associated with ureides accumulation. To identify genetic variation of common bean in response to drought stress, changes in the expression of ALLANTONAISE (PvALN) gene and ureides content were examined in the leaf tissues of the three common bean genotypes (CAL96, DAB514 and DAB541) and one tepary bean genotype (Phaseolus acutifolius A.Gray). Amongst all the genotypes, the suggested drought susceptibility in DAB514 common bean genotype, was probably attributed to a repressed PvALN expression rate which were corroborated by an impaired ureides levels, and reduced plant growth. On contrary, drought stress induced an upregulated relative expression of PvALN coupled with an increase in allantoin and allantoate in DAB541 common bean genotype. In addition, the sustained plant growth in CAL96 was probably attributed to a steady amount of allantoin synthesized under drought stress. Taken together, DAB541 and CAL96 common bean genotypes are the promising genotypes with an induced upregulated transcriptional control of catabolism and/or biosynthesis of ureides, hence potential genotypes for selection and introduction under Botswana semi-arid conditions.


Keywords


common bean; drought stress; ureides: allantonaise; allantoin; allantoate

Full Text:

PDF

References


Alamillo, J. M., Luís Díaz-Leal, J., Victoria Sánchez-Moran, M. A., & Pineda, M. (2010). Molecular analysis of ureide accumulation under drought stress in Phaseolus vulgaris L. Plant, Cell and Environment, 33, 1828–1837. https://doi.org/10.1111/j.1365-3040.2010.02187.x

Beebe, S. E., Rao, I. M., Blair, M. W., & Acosta-Gallegos, J. A. (2013). Phenotyping common beans for adaptation to drought. Frontiers in Physiology, 4 MAR. https://doi.org/10.3389/fphys.2013.00035

Broughton, W. J., Hernández, G., Blair, M., Beebe, S., Gepts, P., & Vanderleyden, J. (2003). Beans (Phaseolus spp.) - Model food legumes. Plant and Soil, 252(1), 55–128. https://doi.org/10.1023/A:1024146710611

Charlson, D. V., Korth, K. L., & Purcell, L. C. (2009). Allantoate amidohydrolase transcript expression is independent of drought tolerance in soybean. Journal of Experimental Botany, 60(3), 847–851. https://doi.org/10.1093/jxb/ern332

Coleto, I., Pineda, M., Rodiñ, O. A. P., De Ron, A. ., & Alamillo, J. (2014). Comparison of inhibition of N2 fixation and ureide accumulation under water deficit in four common bean genotypes of contrasting drought tolerance. Annals of Botany, 113, 1071–1082. https://doi.org/10.1093/aob/mcu029

Díaz-Leal, J. L., Gálvez-Valdivieso, G., Fernández, J., Pineda, M., & Alamillo, J. M. (2012). Developmental effects on ureide levels are mediated by tissue-specific regulation of allantoinase in Phaseolus vulgaris L. Journal of Experimental Botany, 63(11), 4095–4106. https://doi.org/10.1093/jxb/ers090

FANRPAN. (2017). FANRPAN Policy Brief CLIMATE-SMART AGRICULTURE IN BOTSWANA. In Promoting a Conducive Policy Environment for a Food and Nutrition Secure Africa (Issue 2017).

Irani, S., & Todd, C. D. (2016). Ureide metabolism under abiotic stress in Arabidopsis thaliana. Journal of Plant Physiology, 199, 87–95. https://doi.org/10.1016/j.jplph.2016.05.011

King, C. ., & Purcell, L. C. (2005). Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiology, 137, 1389–1396. https://doi.org/10.1104/pp.104.056317

Kohl, D. H., Lin, J. J., Shearer, G., & Schubert, K. R. (1990). Activities of the pentose phosphate pathway and enzymes of proline metabolism in legume root nodules. Plant Physiology, 94(3), 1258–1264. https://doi.org/10.1104/pp.94.3.1258

Ladrera, R., Marino, D., Larrainzar, E., González, E. M., & Arrese-Igor, C. (2007). Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean 1[OA]. Plant Physiology, 145, 539–546. https://doi.org/10.1104/pp.107.102491

Lescano, I. (2020). Determination of ureides content in plant tissues. Bio-Protocol, 10(11), 1–9. https://doi.org/10.21769/bioprotoc.3642

Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/METH.2001.1262

Molosiwa, O. O., Pharudi, J., Seketeme, S., Mashiqa, P., & Chirwa, R. (2019). Assessing yield stability and adaptability of Andean common bean genotypes in the semi-arid environment of Botswana. African Journal of Agricultural Research, 14, 1593–1600. https://doi.org/10.5897/ajar2019.13988

Muñoz, A., Piedras, P., Aguilar, M., & Pineda, M. (2001). Urea is a product of ureidoglycolate degradation in chickpea. Purification and characterization of the ureidoglycolate urea-lyase. Plant Physiology, 125(2), 828–834. https://doi.org/10.1104/pp.125.2.828

Mwale, S. E., Shimelis, H., Mafongoya, P., & Mashilo, J. (2020). Breeding tepary bean (Phaseolus acutifolius) for drought adaptation: A review. Plant Breeding, 139, 821–833. https://doi.org/10.1111/pbr.12806

Pimratch, S., Jogloy, S., Vorasoot, N., Toomsan, B., Patanothai, A., & Holbrook, C. C. (2008). Relationship between biomass production and nitrogen fixation under drought-stress conditions in peanut genotypes with different levels of drought resistance. Journal of Agronomy and Crop Science, 194(1), 15–25. https://doi.org/10.1111/J.1439-037X.2007.00286.X

Purcell, L. C., Serraj, R., SinclairT.R., & DeA. (2004). Soybean N2 fixation estimates, ureide concentration, and yield responses to drought. Crop Science, 44, 484–492. https://doi.org/10.2135/cropsci2004.4840

Serraj, R. (1999). Review article. Symbiotic N2 fixation response to drought. Journal of Experimental Botany, 50(331), 143–155. https://doi.org/10.1093/jexbot/50.331.143

Serraj, Rachid. (2003). Effects of drought stress on legume symbiotic nitrogen fixation: Physiological mechanisms. Indian Journal of Experimental Biology, 41(10), 1136–1141.

Serraj, Rachid, Sinclair, T. R., & Purcell, L. C. (1999). Symbiotic N2 fixation response to drought. Journal of Experimental Botany, 50(331), 143–155. https://doi.org/10.1093/jxb/50.331.143

Serraj, Rachid, Vadez, V., Denison, R. F., & Sinclair, T. R. (1999). Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiology, 119(1), 289–296. https://doi.org/10.1104/pp.119.1.289

Smith, P. M. C., & Atkins, C. A. (2002). Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiology, 128(3), 793–802. https://doi.org/10.1104/pp.010912

Takagi, H., Watanabe, S., Tanaka, S., Matsuura, T., Mori, I. C., Hirayama, T., Shimada, H., & Sakamoto, A. (2018). Disruption of ureide degradation affects plant growth and development during and after transition from vegetative to reproductive stages. BMC Plant Biology, 18(1), 1–16. https://doi.org/10.1186/s12870-018-1491-2

Vadez, V., & Sinclair, T. R. (2001). Leaf ureide degradation and N2 fixation tolerance to water deficit in soybean. Journal of Experimental Botany, 52(354), 153–159. https://doi.org/10.1093/jxb/52.354.153

Watanabe, S., Matsumoto, M., Hakomori, Y., Takagi, H., Shimada, H., & Sakamoto, A. (2013). The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism. https://doi.org/10.1111/pce.12218

Watanabe, S., Matsumoto, M., Hakomori, Y., Takagi, H., Shimada, H., & Sakamoto, A. (2014). The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism. Plant, Cell and Environment, 37(4), 1022–1036. https://doi.org/10.1111/pce.12218

Werner, A. K., Medina-Escobar, N., Zulawski, M., Sparkes, I. A., Cao, F. Q., & Witte, C. P. (2013). The ureide-degrading reactions of purine ring catabolism employ three amidohydrolases and one aminohydrolase in arabidopsis, soybean, and rice. Plant Physiology, 163(2), 672–681. https://doi.org/10.1104/pp.113.224261

Zrenner, R., Stitt, M., Sonnewald, U., & Boldt, R. (2006). Pyrimidine and purine biosynthesis and degradation in plants. Annual Review of Plant Biology, 57, 805–836. https://doi.org/10.1146/annurev.arplant.57.032905.105421




DOI: http://dx.doi.org/10.14720/aas.2022.118.2.2541

Refbacks

  • There are currently no refbacks.


Copyright (c) 2022 Motlalepula PHOLO-TAIT, Thuto KGETSE, Gaone Nthabeleng TSHEKO, Olerato Tsotlhe THEDI, Katso LETHOLA, Ebenezer Oteng MOTLAMME, Moagisi Innocent ITHUTENG, Samodimo NGWAKO

 

Acta agriculturae Slovenica is an Open Access journal published under the terms of the Creative Commons CC BY License.

                           


eISSN 1854-1941