Comparative study of the effect of salt stress, Alternaria alternata attack or combined stress on the Cakile maritima growth and physiological performance

  • Arbia CHALBI Center of Biotechnology of Borj Cedria (CBBC), Laboratory of Extremophile Plants, P. O. Box 901, 2050, Hammam-Lif (TN)
  • Besma SGHAIER-HAMMAMI Center of Biotechnology of Borj Cedria (CBBC), Laboratory of Extremophile Plants, P. O. Box 901, 2050, Hammam-Lif; Laboratoire LR13AGR01, Université De Carthage, Institut National Agronomique de Tunisie, Tunis;Agroforestry and Plant Biochemistry and Proteomics Research Group, Dpt. Biochemistry and Molecular Biology, University of Cordoba-CeiA3, Cordoba (TN)
  • Narjes BAAZAOUI King Khalid University, Abha 61421 (SA)
  • Sofiene B.M. HAMMAMI Laboratoire LR13AGR01, Université De Carthage, Institut National Agronomique de Tunisie, Tunis (TN)
  • Hatem BEN-JOUIRA Center of Biotechnology of Borj Cedria (CBBC), Laboratory of Extremophile Plants, P. O. Box 901, 2050, Hammam-Lif (TN)
  • Pedro GARCÍA-CAPARRÓS Department of Superior School Engineering, University of Almeria, Ctra. Sacramento s/n, La Cañada de San Urbano, 04120 Almería (ES)
  • Naceur DJÉBALI Centre of Biotechnology of Borj Cedria (CBBC), Laboratory of Bioactive Substances, P. O. Box 901, 2050, Hammam-Lif (TN)
  • Imed REGAYA Center of Biotechnology of Borj Cedria (CBBC), Laboratory of Extremophile Plants, P. O. Box 901, 2050, Hammam-Lif; University of Carthage, Higher Institute of Environmental Sciences and Technologies, Borj Cedria (TN)
  • Ahmed DEBEZ Center of Biotechnology of Borj Cedria (CBBC), Laboratory of Extremophile Plants, P. O. Box 901, 2050, Hammam-Lif (TN)
  • Jesús V. JORRÍN-NOVO Agroforestry and Plant Biochemistry and Proteomics Research Group, Dpt. Biochemistry and Molecular Biology, University of Cordoba-CeiA3, Cordoba (ES)
  • Chedly ABDELLY Center of Biotechnology of Borj Cedria (CBBC), Laboratory of Extremophile Plants, P. O. Box 901, 2050, Hammam-Lif (TN)
Keywords: Alternaria alternata, Cakile maritima, combined stress, fungal attack alleviation, salt stress

Abstract

Cakile maritima is a halophytic plant model that is well known by its ability to tolerate high salt concentrations. Salinity was reported to improve the tolerance of halophytes to several abiotic stresses; however, the involvement of salt in the tolerance to biotic stress is still scant. In the present work, the effect of salt on C. maritima responses towards the pathogenic Alternaria alternata was investigated. For that, C. maritima seeds were germinated for four weeks. Plants were then divided into four groups: i) Plants irrigated with salt (200mM NaCl); ii) Plants infested by fungus; iii) Plants irrigated with salt and infested by fungus and finally control plants (0mM NaCl, without inoculation). Our results showed that upon salt stress or fungal attack, plants reduced biomass production, hydration status and photosynthetic performance which were associated with a decrease in the gas exchange and chlorophyll fluorescence parameters, with a more pronounced effect upon fungal attack. However, under combined stress, a significant increase of these parameters was noticed, with a level close to that of control. Concerning nutrient contents, K, Zn, Fe, Cu and Mg decreased in the C. maritima leaves exposed to both stresses applied individually. In contrast, all these nutrients were increased in plants grown under combined stress. Taken together, we can conclude that plants grown under combined stresses had better growth rate and physiological performance compared to all other treated plants, and that salt may be the key in improving the C. maritima ability to tolerate fungal attack.

Metrics

Metrics Loading ...

References

Akimitsu K, Tsuge T, Kodama M, Yamamoto M, Otani H (2014). Alternaria host-selective toxins: Determinant factors of plant disease. Journal of General Plant Pathology 80(2):109-122. https://doi.org/10.1007/s10327-013-0498-7

Álvarez S, Sánchez-Blanco MJ (2015). Comparison of individual and combined effects of salinity and deficit irrigation on physiological, nutritional and ornamental aspects of tolerance in Callistemon laevis plants. Journal of Plant Physiology 1(185):65-74 https://doi.org/10.1016/j.jplph.2015.07.009

Alves AA, Guimarães LM da S, Chaves AR de M, DaMatta FM, Alfenas AC (2011). Leaf gas exchange and chlorophyll a fluorescence of Eucalyptus urophylla in response to Puccinia psidii infection. Acta Physiologiae Plantarum 33(5):1831-1839. https://doi.org/10.1007/s11738-011-0722-z

Arbelet-Bonnin D, Ben-Hamed-Louati I, Laurenti P, Abdelly C, Ben-Hamed K, Bouteau F (2019). Cakile maritima, a promising model for halophyte studies and a putative cash crop for saline agriculture. Advances in Agronomy 155:45-78. https://doi.org/10.1016/bs.agron.2019.01.003

Arntzen CJ (1972). Inhibition of photophosphorylation by tentoxin, a cyclic tetrapeptide. BBA - Bioenergetics 283(3):539-542. https://doi.org/10.1016/0005-2728(72)90273-3

Aveling TAS, Snyman HG, Rijkenberg FHJ (1994). Morphology of infection of onion leaves by Alternaria porri. Canadian Journal of Botany 72(8):1164-1170. https://doi.org/10.1139/b94-142

Ben Amor N, Jiménez A, Boudabbous M, Sevilla F, Abdelly C (2020). Chloroplast implication in the tolerance to salinity of the halophyte Cakile maritima. Russian Journal of Plant Physiology 67(3):507-514. https://doi.org/10.1134/S1021443720030048

Cavaco AR, Matos AR, Figueiredo A (2021). Speaking the language of lipids: the cross-talk between plants and pathogens in defence and disease. Cellular and Molecular Life Sciences 78(9):4399-4415. https://doi.org/10.1007/s00018-021-03791-0

Chalbi A, Sghaier-hammami B, Meca G (2020). Characterization of mycotoxigenic Alternaria species isolated from the Tunisian halophyte Cakile maritima. Phytopathologia Mediterranea 59(1):107-118. https://doi.org/10.14601/Phyto-10720

Chojak-Koźniewska J, Kuźniak E Zimny J (2018). The effects of combined abiotic and pathogen stress in plants: insights from salinity and Pseudomonas syringaepv lachrymans interaction in cucumber. Frontiers in Plant Science 9:1691. https://doi.org/10.3389/fpls.2018.01691

Christophe BG, Hermann P, Séraphin AZ, Agapit DW, Stanley L, David HM, Françoise AK, Armel CGM (2018). Effects of salinity stress on growth in relation to gas exchanges parameters and water status in amaranth (Amaranthus cruentus). International Journal of Plant Physiology and Biochemistry 10(3):19-27. https://doi.org/10.5897/ijppb2018.0280

Davy AJ, Scott R, Cordazzo CV (2006) Biological flora of the British Isles: Cakile maritima Scop. Journal of Ecology 94:695-711. https://doi.org/10.1111/j.1365-2745.2006.01131.x

Debez A, Rejeb K Ben,Ghars MA, Gandour M, Megdiche W, Hamed K Ben, Amor N Ben, Brown SC, Savouré A, Abdelly C (2013). Ecophysiological and genomic analysis of salt tolerance of Cakile maritima. Environmental and Experimental Botany 92:64-72. https://doi.org/10.1016/j.envexpbot.2012.12.002

Demirbas S, Acar O (2017). Physiological and biochemical defense reactions of Arabidopsis thaliana to phelipanche ramosa infection and salt stress. Fresenius Environmental Bulletin 26(3):2268-2275.

Draper HH, Hadley M (1990). Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology 186(C):421-431. https://doi.org/10.1016/0076-6879(90)86135-I

Ellouzi H, Ben Hamed K, Asensi-Fabado MA, Müller M, Abdelly C, Munné-Bosch S (2013). Drought and cadmium may be as effective as salinity in conferring subsequent salt stress tolerance in Cakile maritima. Planta 237(5):1311-1323. https://doi.org/10.1007/s00425-013-1847-7

Evelin H, Kapoor Rand Giri B (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Annals of Botany 104(7):1263-1280. https://doi.org/10.1093/aob/mcp251

Farhat N, Kouas W, Braun H-P, Debez A (2021). Stability of thylakoid protein complexes and preserving photosynthetic efficiency are crucial for the successful recovery of the halophyte Cakile maritima to high salinity. Plant Physiology and Biochemistry 166:177-190. https://doi.org/10.1016/j.plaphy.2021.05.044

Flowers TJ, Colmer TD (2008). Salinity tolerance in halophytes. New Phytologist 179(4):945-963. https://doi.org/10.1111/j.1469-8137.2008.02531.x

Flowers TJ, Colmer TD (2015). Plant salt tolerance: Adaptations in halophytes. Annals of Botany 115(3):327-331. https://doi.org/10.1093/aob/mcu267

Ghnaya T, Nouairi I, Slama I, Messedi D, Grignon C, Abdelly C, Ghorbel MH (2005). Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. Journal of Plant Physiology 162(10):1133-1140. https://doi.org/10.1016/j.jplph.2004.11.011

Gil R, Lull C, BoscaiuM, Bautista I, Lidón A, Vicente O (2011). Soluble carbohydrates as osmolytes in several halophytes from a Mediterranean salt marsh. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 39(2):9-17. https://doi.org/10.15835/nbha3927176

Giri P, Taj G, Meena P D, Kumar A, Pradesh U (2013). Microscopic study of Alternaria brassicae infection processes in Brassica juncea cultivars by drop plus agarose method. African Journal of Microbiology Research 7(33):4284-4290. https://doi.org/10.5897/AJMR2013.5585

Gleick P H, Christian-Smith J, Cooley H (2011). Water-use efficiency and productivity: Rethinking the basin approach. Water International 36(7):784-798. https://doi.org/10.1080/02508060.2011.631873

Glenn EP, Nelson SG, Ambrose B, MartinezR, Soliz D, Pabendinskas V, Hultine K (2012). Comparison of salinity tolerance of three Atriplex spp. in well-watered and drying soils. Environmental and Experimental Botany 82:62-72. https://doi.org/10.1016/j.envexpbot.2012.04.010

Gupta VP, Raju HV, Kumar V, Govindaiah (1998). Surface ultrastructure of infection process of Alternaria alternata and Fusarium pallidoroseum on mulberry. Archives of Phytopathology and Plant Protection 31(5):429-434. https://doi.org/10.1080/03235409809383254

Hamed K Ben, Ellouzi H, Talbi O Z, Hessini K, Slama I, Ghnaya T, Bosch SM, Savouré A, Abdelly C (2013). Physiological response of halophytes to multiple stresses. Functional Plant Biology 40(9):883-896. https://doi.org/10.1071/FP13074

Hassan M Al, Chaura J, Donat-Torres MP, Boscaiu M, Vicente O (2017). Antioxidant responses under salinity and drought in three closely related wild monocots with different ecological optima. AoB PLANTS 9:plx009. https://doi.org/10.1093/aobpla/plx009

Hewitt EJ, Eden A (1953). Sand and water culture methods used in the study of plant nutrition. The Analyst 78(926):329-330. https://doi.org/10.2136/sssaj1966.03615995003000040002x

Mamgain A, Biswas MK (2020). Impact of different environmental factors on the progression of Alternaria blight of mustard caused by Alternaria brassicae. Alochana Chakra Journal IX(V):6843-6859.

Manzoor Alam S (1999). Nutrient uptake by plants under stress conditions. Handbook of Plant and Crop Stress 2:285-313. https://doi.org/10.1201/9780824746728.ch12

Meena M, Samal S (2019). Alternaria host-specific (HSTs) toxins: An overview of chemical characterization, target sites, regulation and their toxic effects. Toxicology Reports 6:745-758. https://doi.org/10.1016/j.toxrep.2019.06.021

Megdiche W, Amor N Ben, Debez A, Hessini K, Ksouri R, Zuily-Fodil Y, Abdelly C (2007). Salt tolerance of the annual halophyte Cakile maritima as affected by the provenance and the developmental stage. Acta Physiologiae Plantarum 29(4):375-384. https://doi.org/10.1007/s11738-007-0047-0

Mohammadi Alagoz S, Toorchi M, Bandehagh A (2016). Canola seedling response to NaCl stress - a proteomic approach. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 44(2):361-366. https://doi.org/10.15835/nbha44210462

Mohsin SM, Islam MR, Ahmmed ANF, Nisha HAC, Hasanuzzaman M (2016). Cultural, morphological and pathogenic characterization of alternaria porri causing purple blotch of onion. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 44(1):222-227. https://doi.org/10.15835/nbha44110110

Møller IM, Jensen PE, Hansson A (2007). Oxidative modifications to cellular components in plants. Annual Review of Plant Biology 58:459-481. https://doi.org/10.1146/annurev.arplant.58.032806.103946

Polanco LR, Rodrigues FA, Nascimento KJT, Cruz MFA, Curvelo CRS, DaMatta FM, Vale FXR (2014). Photosynthetic gas exchange and antioxidative system in common bean plants infected by Colletotrichum lindemuthianum and supplied with silicon. Tropical Plant Pathology 39(1):35-42. https://doi.org/10.1590/S1982-56762014000100005

Qiu N, Lu Q, Lu C (2003). Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex centralasiatica. New Phytologist 159(2):479-486. https://doi.org/10.1046/j.1469-8137.2003.00825.x

Ribeiro RV, Machado EC, Oliveira RF (2004). Growth- and leaf-temperature effects on photosynthesis of sweet orange seedlings infected with Xylella fastidiosa. Plant Pathology 53(3):334-340. https://doi.org/10.1111/j.0032-0862.2004.01012.x

Schreiber U, Ulrich S (2004). Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Chlorophyll a fluorescence 279-319. https://doi.org/10.1300/j301v01n03_06

Scott DC, Lawrence C (2008). The cell wall integrity-associated map kinase homolog, AbSlt2 in the ecrotrophic fungus Alternaria brassicicola is required for pathogenicity of Brassicas. Masters Theses [20058]. http://hdl.handle.net/10919/31203

Sharov AA, Dudekula DB, Ko MSH (2005). A web-based tool for principal component and significance analysis of microarray data. Bioinformatics 15(10):2548-2549. https://doi.org/10.1093/bioinformatics/bti343

Shiri M, Rabhi M, El Amrani A, Abdelly C (2015). Cross-tolerance to abiotic stresses in halophytes: application for phytoremediation of organic pollutants. Acta Physiologiae Plantarum 37(10). https://doi.org/10.1007/s11738-015-1954-0

Sinha M, Singh RP, Kushwaha GS, Iqbal N, Singh A, Kaushik S, Kaur P, Sharma S, Singh TP (2014). Current overview of allergens of plant pathogenesis related protein families. The Scientific World Journal. https://doi.org/10.1155/2014/543195

Slama I, Ghnaya T, Messedi D, Hessini K, Labidi N, Savoure A, Abdelly C (2007). Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grown in mannitol-induced water stress. Journal of Plant Research 120(2):291-299. https://doi.org/10.1007/s10265-006-0056-x

Sobczak M, Skoczowski A, Oliwa J, Kononowicz AK (2020). Complexity of Brassica oleracea – Alternaria brassicicola susceptible interaction reveals downregulation of photosynthesis at ultrastructural, transcriptional, and physiological levels. Cells 9(10):2329.

Sogoni A, Jimoh M, Kambizi L, Laubscher C (2021). The impact of salt stress on plant growth, mineral composition, and antioxidant activity in Tetragonia decumbens Mill.: An underutilized edible halophyte in South Africa. Horticulturae 7(6):140. https://doi.org/10.3390/horticulturae7060140

Somma S, Amatulli MT, Masiello M, Moretti A, Logrieco AF (2019). Alternaria species associated to wheat black point identified through a multilocus sequence approach. International Journal of Food Microbiology 293:34-43. https://doi.org/10.1016/j.ijfoodmicro.2019.01.001

Vloutoglou I, Fitt BDL, Lucas JA (1996). Germination of Alternaria linicola conidia on linseed: Effects of temperature, incubation time, leaf wetness and light regime. Plant Pathology 45(3):529-539. https://doi.org/10.1046/j.1365-3059.1996.d01-2.x

Wided M, Nader BA, Debez A, Kamel H, Riadh K, Chedly A (2009). Physiological and biochemical traits involved in the genotypic variability to salt tolerance of Tunisian Cakile maritima. African Journal of Ecology 47(4):774-783. https://doi.org/10.1111/j.1365-2028.2009.01073.x

Yang ZX, Yang YF, Yu SZ, Wang RG, Wang Y, Chen HL (2018). Photosynthetic, photochemical and osmotic regulation changes in tobacco resistant and susceptible to Alternaria alternata.Tropical Plant Pathology 43(5):413-421. https://doi.org/10.1007/s40858-018-0222-4

Zarrouk M, El Almi H, Ben Youssef, Sleimi N, Smaoui A, Ben Miled, Abdelly C (2003) Lipid composition of local halophytes seeds: Cakile maritima, Zygophyllum album and Crithmum maritimum. In: Crash Crop Halophytes: Recent Studies. 10 Years After the Al Ain (Ed. H. Lieth). Klumer Academic Publishers Group, Dordrecht.

Zribi OT, Labidi N, Slama I, Debez A, Ksouri R, Rabhi M, Smaoui A, Abdelly C (2012). Alleviation of phosphorus deficiency stress by moderate salinity in the halophyte Hordeum maritimum L. Plant Growth Regulation 66(1):75-85. https://doi.org/10.1007/s10725-011-9631-9

Xu ZZ, Zhou GS, Han G, Li Y (2011). Photosynthetic potential and its association with lipid peroxidation in response to high temperature at different leaf ages in maize. Journal of Plant Growth Regulation 30:41-50. https://doi.org/10.1007/s00344-010-9167-7

Xu ZZ, Zhou GS, Shimizu H (2009). Effects of soil drought with nocturnal warming on leaf stomatal traits and mesophyll cell ultrastructure of a perennial grass. Crop Science 49:1843-1851. https://doi.org/10.2135/cropsci2008.12.0725

Published
2021-09-28
How to Cite
CHALBI, A., SGHAIER-HAMMAMI, B., BAAZAOUI, N., HAMMAMI, S. B., BEN-JOUIRA, H., GARCÍA-CAPARRÓS, P., DJÉBALI, N., REGAYA, I., DEBEZ, A., JORRÍN-NOVO, J. V., & ABDELLY, C. (2021). Comparative study of the effect of salt stress, Alternaria alternata attack or combined stress on the Cakile maritima growth and physiological performance. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(3), 12446. https://doi.org/10.15835/nbha49312446
Section
Research Articles
CITATION
DOI: 10.15835/nbha49312446