ISHS
  Fruits
     
Fruits
Home


Submit
an article


Subscriptions

ISHS Home

ISHS Contact

Search

Fruits
  Fruits 75 (5) 204-215 | DOI: 10.17660/th2020/75.5.3
ISSN 0248-1294 print and 1625-967X online | © ISHS 2020 | Fruits, The International Journal of Tropical and Subtropical Horticulture | Original article

Efficient compartmentalization and translocation of toxic minerals lead tolerance in volkamer lemon tetraploids more than diploids under moderate and high salt stress

Muhammad Fasih Khalid1,2, Sajjad Hussain1,a, Muhammad Akbar Anjum1, Muhammad Arif Ali3, Shakeel Ahmad4, Shaghef Ejaz1, Sajid Ali1, Muhammad Usman5, Ehsan Ul Haque6 and R. Morillon7
1 Department of Horticulture, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan
2 Citrus Research and Education Centre, University of Florida, 33850 Lake Alfred, FL, United States
3 Department of Soil Science, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan
4 Department of Agronomy, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan
5 Institute of Horticultural Sciences, University of Agriculture, Faisalabad, Pakistan
6 Citrus Research Institute, Sargodha, Pakistan
7 Equpie “Structure Evolutive des Agrumes, Polyploidie et Amelioration Genetique”, SEAPAG – CIRAD, UMR AGAP, F-97170 Petit-Bourg, Guadeloupe, France – AGAP, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France

SUMMARY
Introduction – Salt stress affects the growth and development of many crops. Citrus is a major global fruit crop and its production is strictly affected by salinity. The use of polyploid citrus rootstocks has been proposed as a strategy to improve salt tolerance. Although tetraploid rootstocks have been found to be more salt tolerant under low and moderate salinity. But, the mechanisms of these dynamics are unknown, including how they compartmentalize the toxic ions under moderate and high saline soils. Materials and methods – Exploring the differences in salt tolerance mechanism between tetraploid and diploid volkamer lemon rootstock, the plants were exposed to moderate (75 mM) and high (150 mM) salinity for 80 days. Various growth parameters (plant height and diameter, leaves number, dry biomass) and various minerals nutrients (N, P, K, Ca, Na and Cl) in leaves and roots of diploid and tetraploid rootstock were studied to understand tolerance mechanism. Results – The results exhibited that tetraploid rootstock behaved differently to cope with the salinity as compared to diploid. In both diploid and tetraploid rootstocks various growth traits were decreased under moderate and high salinity compared to the control. However the decrement was less in tetraploid as compared to diploid rootstocks in moderate and interestingly in high salinity. Conclusion – Tetraploid and diploid rootstocks compartmentalize the toxic ions differentially and/or different parts against moderate and high salt stress. These results suggest that the use of tetraploid citrus rootstocks will be useful and more beneficial for citrus cultivation in moderate and more importantly high saline soils.

Keywords citrus rootstock, nutrients, polyploidy, salinity, toxicity

Significance of this study

What is already known on this subject?

  • Salinity is one of the major causes of yield decrease of many fruit crops including citrus. Citrus is the major fruit crop of the world but its production is decreasing by different factors, i.e., salinity. Chloride is toxic for citrus. Tetraploids are more tolerant than diploids under moderate salt stress, however, under high salt level, diploids are more tolerant than tetraploids.
What are the new findings?
  • Volkamer lemon tetraploids are more tolerant than diploids under moderate and specifically high salinity. The compartmentalization of toxic ions occur particularly in leaves under moderate salinity and in roots under high salt stress.
What is the expected impact on horticulture?
  • The use of tetraploid rootstocks under moderate and high salt affected soils is a good strategy for better citrus production.

Download fulltext version How to cite this article       Export citation to RIS format      

E-mail: sajjad.hussain@bzu.edu.pk  

References

  • Aleza, P., Froelicher, Y., Schwarz, S., Agusti, M., Hernandez, M., Juarez, J., Luro, F., Morillon, R., Navarro, L., and Ollitrault, P. (2011). Tetraploidization events by chromosome doubling of nucellar cells are frequent in apomictic citrus and are dependent on genotype and environment. Ann. Bot. 108, 37–50. https://doi.org/10.1093/aob/mcr099.

  • Allario, T., Brumos, J., Colmenero-Flores, J.M., Iglesias, D.J., Pina, J.A., Navarro, L., Talon, M., Ollitrault, P., and Morillon, R. (2013). Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell Environm. 36, 856–868. https://doi.org/10.1111/pce.12021.

  • Anjum, M.A. (2008). Effect of NaCl concentration in irrigation water on growth and polyamine metabolism in two citrus rootstocks with different levels of salinity tolerance. Acta Physiol. Plant. 30, 43–52. https://doi.org/10.1007/s11738-007-0089-3.

  • Brumos, J., Colmenero-Flores, J.M., Conesa, A., Izquierdo, P., Sanchez, G., Iglesias, D.J., Lopez-Climent, M.F., Gomez-Cadenas, A., and Talon, M. (2009). Membrane transporters and carbon metabolism implicated in chloride homeostasis differentiate salt stress responses in tolerant and sensitive Citrus rootstocks. Funct. Integr. Genomics 9, 293–309. https://doi.org/10.1007/s10142-008-0107-6.

  • Byrt, C.S., and Munns, R. (2008). Living with salinity. New Phytol. 179, 903–905. https://doi.org/10.1111/j.1469-8137.2008.02596.x.

  • Fatima, B., Usman, M., Khan, I.A., Khan, M.S., and Khan, M.M. (2015). Identification of citrus polyploids using chromosome count, morphological and SSR markers. Pak. J. Agric. Sci. 52, 107–114.

  • Forner-Giner, M.A., Legaz, F., Primo-Millo, E., and Forner, J.B. (2011). Nutritional responses of rootstocks to salinity: performance of the new hybrids, Forner-Alcaide 5 and Forner-Alcaide 13. J. Plant Nutr. 34, 1–16. https://doi.org/10.1080/01904167.2011.585202.

  • Garcia-Sanchez, F., Martinez, V., Jifon, J., Syvertsen, J.P., and Grosser, J.W. (2002). Salinity reduces growth, gas exchange, chlorophyll and nutrient concentrations in diploid sour orange and related allotetraploid somatic hybrids. J. Hortic. Sci. Biotechnol. 77, 379–386. https://doi.org/10.1080/14620316.2002.11511509.

  • Gomez, K.A., and Gomez, A.A.S. (1984). Statistical Procedures for Agricultural Research (New York, USA: Wiley).

  • Grosser, J.W., Omar, A.A., Gmitter, J.A., and Syvertsen, J.P. (2012). Salinity tolerance of Valencia orange trees on allotetraploid rootstocks. In Proceedings of Florida State Horticulture Society (Florida, US) 125, 50–55.

  • Hatfield, J.L., and Prueger, J.H. (2015). Temperature extremes: Effect on plant growth and development. Weather Clim. Extremes 10, 4–10. https://doi.org/10.1016/j.wace.2015.08.001.

  • Hussain, S., Curk, F., Dhuique-Mayer, C., Urban, L., Ollitrault, P., Luro, F., and Morillon, R. (2012a). Autotetraploid trifoliate orange (Poncirus trifoliata) rootstocks do not impact clementine quality but reduce fruit yields and highly modify rootstock/scion physiology. Sci. Hortic. 134, 100–107. https://doi.org/10.1016/j.scienta.2011.11.008.

  • Hussain, S., Luro, F., Costantino, G., Ollitrault, P., and Morillon, R. (2012b). Physiological analysis of salt stress behaviour of citrus species and genera: Low chloride accumulation as an indicator of salt tolerance. South Afr. J. Bot. 81, 103–112. https://doi.org/10.1016/j.sajb.2012.06.004.

  • Hussain, S., Morillon, R., Anjum, M.A., Ollitrault, P., Costantino, G., and Luro, F. (2015). Genetic diversity revealed by physiological behavior of citrus genotypes subjected to salt stress. Acta Physiol. Plant. 37, 1–10. https://doi.org/10.1007/s11738-014-1740-4.

  • Hussain, S., Khalid, M.F., Hussain, M., Ali, M.A., Nawaz, A., Zakir, I., Fatima, Z., and Ahmad, S. (2018). Role of micronutrients in salt stress tolerance to plants. In Plant Nutrients and Abiotic Stress Tolerance, M. Hasanuzzaman, M. Fujita, H. Oku, K. Nahar, and B. Hawrylak-Nowak, eds. (Singapore: Springer), p. 363–376. https://doi.org/10.1007/978-981-10-9044-8_15.

  • Khalid, M.F., Hussain, S., Ahmad, S., Ejaz, S., Zakir, I., Ali, M.A., Ahmed, N., and Anjum, M.A. (2019). Impacts of abiotic stresses on growth and development of plants. In Plant Tolerance to Environmental Stress, M. Hasanuzzaman, M. Fujita, H. Oku, and M.T. Islam, eds. (USA: CRC Press), pp. 1–8. https://doi.org/10.1201/9780203705315-1.

  • Khalid, M.F., Hussain, S., Anjum, M.A., Ahmad, S., Ali, M.A., Ejaz, S., and Morillon, R. (2020). Better salinity tolerance in tetraploid vs. diploid volkamer lemon seedlings is associated with robust antioxidant and osmotic adjustment mechanisms. J. Plant Physiol. 244, 153071. https://doi.org/10.1016/j.jplph.2019.153071.

  • Khoshbakht, D., Ramin, A.A., and Baninasab, B. (2015). Effects of sodium chloride stress on gas exchange, chlorophyll content and nutrient concentrations of nine citrus rootstocks. Photosynthetica 53, 241–249. https://doi.org/10.1007/s11099-015-0098-1.

  • Lea-Cox, J.D., and Syvertsen, J.P. (1993). Salinity reduces water use and nitrate-N-use efficiency of citrus. Ann. Bot. 72, 47–54. https://doi.org/10.1006/anbo.1993.1079.

  • Martin, F., Winspear, M.J., MacFarlane, J.D., and Oaks, A. (1983). Effect of methionine sulfoximine on the accumulation of ammonia in C3 and C4 leaves: The relationship between NH3 accumulation and photorespiratory activity. Plant Physiol. 71, 177–181. https://doi.org/10.1104/pp.71.1.177.

  • Mouhaya, W., Allario, T., Brumos, J., Andres, F., Froelicher, Y., Luro, F., Talon, M., Ollitrault, P., and Morillon, R. (2010). Sensitivity to high salinity in tetraploid citrus seedlings increases with water availability and correlates with expression of candidate genes. ‎Funct. Plant Biol. 37, 674–685. https://doi.org/10.1071/FP10035.

  • Moya, J.L., Gómez-Cadenas, A., Primo-Millo, E., and Talon, M. (2003). Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. J. Exp. Bot. 54, 825–833. https://doi.org/10.1093/jxb/erg064.

  • Munns, R., and Tester, M. (2008). Mechanisms of salt tolerance. Annu. Rev. Plant Biol. 59, 651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911.

  • Ohno, T., and Zibilske, L.M. (1991). Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55, 892–895. https://doi.org/10.2136/sssaj1991.03615995005500030046x.

  • Oustric, J., Morillon, R., Luro, F., Herbette, S., Lourkistia, R., Giannettinia, J., Berti, L., and Santini, J. (2017). Tetraploid Carrizo citrange rootstock (Citrus sinensis Osb. × Poncirus trifoliata L. Raf.) enhances natural chilling stress tolerance of common clementine (Citrus clementina Hort. ex Tan). J. Plant Physiol. 214, 108–115. https://doi.org/10.1016/j.jplph.2017.04.014.

  • Perez-Perez, J.G., Syvertsen, J.P., Botía, P., and García-Sanchez, F. (2007). Leaf water relations and net gas exchange responses of salinized Carrizo citrange seedlings during drought stress and recovery. Ann. Bot. 100, 335–345. https://doi.org/10.1093/aob/mcm113.

  • Qadir, M., and Schubert, S. (2002). Degradation processes and nutrient constraints in sodic soils. Land Degrad. Dev. 13, 275–294. https://doi.org/10.1002/ldr.504.

  • Romero-Aranda, R., Bondada, B.R., Syvertsen, J.P., and Grosser, J.W. (1997). Leaf characteristics and net gas exchange of diploid and autotetraploid citrus. Ann. Bot. 79, 153–160. https://doi.org/10.1006/anbo.1996.0326.

  • Ruiz, M., Quiñones, A., Martínez-Alcántara, B., Aleza, P., Morillon, R., Navarro, L., Primo-Millo, E., and Martínez-Cuenca, M.R. (2016a). Effects of salinity on diploid (2x) and doubled diploid (4x) Citrus macrophylla genotypes. Sci. Hortic. 207, 33–40. https://doi.org/10.1016/j.scienta.2016.05.007.

  • Ruiz, M., Quiñones, A., Martínez-Cuenca, M.R., Aleza, P., Morillon, R., Navarro, L., Primo-Millo, E., and Martínez-Alcántara, B. (2016b). Tetraploidy enhances the ability to exclude chloride from leaves in carrizo citrange seedlings. J. Plant Physiol. 205, 1–10. https://doi.org/10.1016/j.jplph.2016.08.002.

  • Ryan, J., Estefan, G., and Rashid, A. (2001). Soil and Plant Analysis: Laboratory Manual, 2nd edn. (Aleppo, Syria: International Center for Agriculture Research in the Dry Areas, and Islamabad, Pakistan: National Agriculture Research Center), 15, 71–76.

  • Saleh, B., Allario, T., Dambier, D., Ollitrault, P., and Morillon, R. (2008). Tetraploid citrus rootstocks are more tolerant to salt stress than diploid. C. R. Biol. 331, 703–710. https://doi.org/10.1016/j.crvi.2008.06.007.

  • Syvertsen, J.P., and García-Sanchez, F. (2014). Multiple abiotic stresses occurring with salinity stress in citrus. Environm. Exp. Bot. 103, 128–137. https://doi.org/10.1016/j.envexpbot.2013.09.015.

  • Tan, F.Q., Tu, H., Liang, W.J., Long, J.M., Wu, X.M., Zhang, H.Y., and Guo, W.W. (2015). Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biol. 15, 89. https://doi.org/10.1186/s12870-015-0450-4.

  • Yahmed, J.B., de Oliveira, T.M., Novillo, P., Quinones, A., Forner, M.A., Salvador, A., Froelicher, Y., Mimoun, M.B., Talon, M., Ollitrault, P., and Morillon, R. (2016). A simple, fast and inexpensive method to assess salt stress tolerance of aerial plant part: Investigations in the mandarin group. J. Plant Physiol. 190, 36–43. https://doi.org/10.1016/j.jplph.2015.10.008.

Received: 10 March 2020 | Accepted: 27 June 2020 | Published: 24 September 2020 | Available online: 24 September 2020

previous article     Volume 75 issue 5     next article