Abstract
Salinity stress in increasingly becoming a major challenge in current and expanding agricultural ecosystems. Unlike temporal abiotic stresses, plants are usually exposed to salinity stress for an entire lifespan. Therefore, a long term effect (10 weeks) of continuous salinity exposure was investigated for three common fig landraces (Zraki, Mwazi, and Khdari). Both relative water content and chlorophyll content decreased with elevated salinity stress, while stem length barely changed. The most prominent decline was observed in root biomass. The data would align common fig to moderately tolerant threshold slop with a C50 range of 100 to 150 mM NaCl. A high and significant correlation was evident between root biomass and chlorophyll content (85%). Concurrently, differential expression of putative salinity responsive genes in common fig were determined; signal peptide peptidase-like 2B (FcSPPL2B), dehydration responsive element binding protein (FcDREB), calcineurin B-like protein (CBL)-CBL-interacting serine/threonine-protein kinase 11 (FcCIPK11), sorbitol dehydrogenase (FcSORD) and dehydrin (FcDHN). The data were discussed for each gene in respect of its potential role in salinity stress mitigation. The combined physiological and molecular data would conclude Zraki as the most salinity tolerant genotype. The major implication of the data emphasizes the tremendous genotype by environment (salinity stress) interaction in common fig.
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References
Abdel-Razik MS, El-Darier S (1991) Functional adaptations of fig trees (Ficus carica L.) In agroecosystems of the western Mediterranean Desert of Egypt. Qatar Univ Sci J 11:183–199
Alcamo J (2019) Water quality and its interlinkages with the sustainable development goals. Curr Opin Environ Sustain 36:126–140
Ali-Shtayeh MS, Jamous RM, Zaitoun SYA, Mallah OB, Mubaslat AK (2014) Genetic diversity of the Palestinian fig (Ficus carica L.) collection by pomological traits and RAPD markers. Am J Plant Sci 5:1139
Almajali DA, Abdel-Ghani AH, Migdadi H (2012) Evaluation of genetic diversity among Jordanian fig germplasm accessions by morphological traits and ISSR markers. Sci Hortic 147:8–19
Amarasinghe S, Watson-Haigh NS, Gilliham M, Roy S, Baumann U (2016) The evolutionary origin of CIPK16: a gene involved in enhanced salt tolerance. Mol Phylogenet Evol 100:135–147
Asakura T, Hoshi M. 2015. Activation of plant signal peptide peptidase by saline solutions. In: Analyzing the effect of salts on regulation of food-related metalloenzymes for verification of its significance in food processing and cooking. The salt science research foundation. Tokyo, Japan.
Ateyyeh AF, Sadder MT (2006a) Growth pattern and fruit characteristics of six common fig (Ficus carica L.) cultivars in Jordan. Jordan J Agric Sci 2:105–112
Ateyyeh AF, Sadder MT (2006b) Preliminary study on the vegetative and reproductive growth of six common fig (Ficus carica L.) cultivars in Jordan. Jordan J Agric Sci 2:1–7
Bahmani K, Noori SAS, Darbandi AI, Akbari A (2015) Molecular mechanisms of plant salinity tolerance: a review. Aust J Crop Sci 9:321
Bernstein N, Meiri A, Zilberstaine M (2004) root growth of avocado is more sensitive to salinity than shoot growth. J Am Soc Hortic Sci 129:188–192
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622
Caruso G, Gennai C, Ugolini F, Marchini F, Quartacci MF, Gucci R (2017) Tolerance and physiological response of young Ficus carica L. plants irrigated with saline water. Acta Hortic 1173:137–141
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Ana Biochem 162:156–159
Cimato A, Castelli S, Tattini M, Traversi ML (2010) An ecophysiological analysis of salinity tolerance in olive. Environ Exp Bot 68:214–221
Costa F, Marchese A, Mafrica R et al (2017) Genetic diversity of fig (Ficus carica L.) genotypes grown in Southern Italy revealed by the use of SSR markers. Acta Hortic 1173:75–80
Darwish AD, El-Berry IM, Mustafa NS, Moursy FS, Hagagg LF (2015) Detecting drought tolerance of fig (Ficus carica L.) cultivars depending on vegetative growth and peroxidase activity. Int J ChemTech Res 8:1520–1532
Deguchi M, Bennett AB, Yamaki S, Yamada K, Kanahama K, Kanayama Y (2006) An engineered sorbitol cycle alters sugar composition, not growth, in transformed tobacco. Plant Cell Environ 29:1980–1988
El-Shazly SM, Mustafa NS, El-Berry IM (2014) Evaluation of some fig cultivars grown under water stress conditions in newly reclaimed soils. Middle-East J Sci Res 21:1167–1179
Felsenstein J (1989) PHYLIP - phylogeny inference package (Version 3.2). Cladistics 5:164–166
Fuglsang AT, Guo Y, Cuin TA et al (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634
Garg R, Shankar R, Thakkar B, Kudapa H, Krishnamurthy L, Mantri N, Varshney RK, Bhatia S, Jain M (2016) Transcriptome analyses reveal genotype-and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Sci Rep 6:19228
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids S 41:95–98
Hanin M, Brini F, Ebel C, Toda Y, Masmoudi TS (2011) Plant dehydrins and stress tolerance versatile proteins for complex mechanisms. Plant Signal Behav 6(10):1503–1509
Haubensak KA, D’Antonio CM, Embry S, Blank R (2014) A comparison of Bromus tectorum growth and mycorrhizal colonization in salt desert vs. sagebrush habitats. Rangeland Ecol Manage 67:275–284
Hishida M, Ascencio-Valle F, Fujiyama H, Endo T, Orduño-Cruz A, Larrinaga-Mayoral JÁ (2013) Response to salt stress in growth, water relations, and ion content of Jatropha curcas and J. cinerea seedlings. Interciencia 38:298–304
Hoshi M, Ohki Y, Ito K, Tomita T, Iwatsubo T, Ishimaru Y, Abe K, Asakura T (2013) Experimental detection of proteolytic activity in a signal peptide peptidase of Arabidopsis thaliana. BMC Biochem 14:16
Huang S, Jiang S, Liang J, Chen M (2019) Roles of plant CBL? CIPK systems in abiotic stress responses. Turk J Bot 43:271–280
Karimi S, Rahemi M, Maftoun M, Eshghi S, Tavallali V (2009) Effects of long-term salinity on growth and performance of two pistachio (Pistacia vera L.) rootstocks. Aust J Basic Appl Sci 3:1630–1639
Khan A, Shafi M, Bakht J, Khan MO, Anwar S (2019) response of wheat varieties to salinity stress as ameliorated by seed priming. Pak J Bot 51:1969–1978
Khanna-Chopra R, Semwal VK, Lakra N, Pareek A (2019) 5 Proline–A key regulator conferring plant tolerance to salinity and drought. In: Hasanuzzaman M, Fujita M, Oku H, Islam MT, eds., Plant tolerance to environmental stress: role of phytoprotectants. CRC Press, Boca Raton.
Kislev ME, Hartmann A, Bar-Yosef O (2006) Early domesticated fig in the Jordan Valley. Sci 312:1372–1374
Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Li P, Zheng T, Li L, Zhuo X, Jiang L, Wang J, Cheng T, Zhang Q (2019) Identification and comparative analysis of the CIPK gene family and characterization of the cold stress response in the woody plant Prunus mume. PeerJ 7:e6847
Li R, Zhang J, Wei J, Wang H, Wang Y, Ma R (2009) Functions and mechanisms of the CBL–CIPK signaling system in plant response to abiotic stress. Pro Nat Sci 19:667–676
Li W, Khan MA, Zhang X, Liu X (2010) Rooting and Shoot growth of stem cutting of saltcedar (Tamareix chinesis Lour) under salt stress. Pak J Bot 42:4133–4142
Litalien A, Zeeb B (2019) Curing the earth: a review of anthropogenic soil salinization and plant-based strategies for sustainable mitigation. Sci Total Environ 698:134235
Liu Y, Ji D, Turgeon R, Chen J, Lin T, Huang J, Luo J, Zhu Y, Zhang C, Lv Z (2019) Physiological and proteomic responses of mulberry trees (Morus alba L.) to combined salt and drought stress. Int J Mol Sci 20:2486
Maas EV, Hoffman GJ (1977) Crop salt tolerance–current assessment. J Irrig Drain Div 103:115–134
Martínez JP, Lutts S, Schanck A, Bajji M, Kinet JM, (2004) Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L? J Plant Physiol 161:1041–1051
McNabb DE (2019) Agriculture and inefficient water use. In: McNabb DE (ed) Global pathways to water sustainability. Springer, New York, pp 99–115
Mentrup T, Loock AC, Fluhrer R, Schröder B (2017) Signal peptide peptidase and SPP-like proteases-Possible therapeutic targets? Biochim Biophys Acta (BBA)-Mol Cell Res 1864:2169–2182.
Metwali EM, Hemaid IAS, Al-Zahrani HS, Howlader SM, Fuller MP (2014) Influence of different concentrations of salt stress on in vitro multiplication of some fig (Ficus carcia L.) cultivars. Life Sci J 11:386–397
Mirck J, Zalesny RS (2015) Mini-review of knowledge gaps in salt tolerance of plants applied to willows and poplars. Int J Phytoremediat 17:640–650
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
NCBI (2019) The National Center for Biotechnology Information. https://www.ncbi.nlm.nih.gov/
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Pommerrenig B, Papini-Terzi FS, Sauer N (2007) Differential regulation of sorbitol and sucrose loading into the phloem of Plantago major in response to salt stress. Plant Physiol 144:1029–1038
Rewald B, Raveh E, Gendler T, Ephrath JE, Rachmilevitch S (2012) Phenotypic plasticity and water flux rates of Citrus root orders under salinity. J Exp Bot 63:2717–2727
Rewald B, Shelef O, Ephrath JE, Rachmilevitch S (2013) Adaptive plasticity of salt-stressed root systems. In: Azooz MM, Prasad MNV (eds) Ahmad P. Ecophysiology and responses of plants under salt stress Springer, New York, pp 169–201
Romero-Trigueros C, Vivaldi GA, Nicolás EN, Paduano A, Salcedo FP, Camposeo S (2019) Ripening indices, olive yield and oil quality in response to irrigation with saline reclaimed water and deficit strategies. Front Plant Sci 10:1243
Roy SJ, Huang W, Wang XJ, Evrard A, Schmöckel SM, Zafar ZU, Tester M (2013) A novel protein kinase involved in Na+ exclusion revealed from positional cloning. Plant Cell Environ 36:553–568
Sadder MT, Ateyyeh AF (2006) Molecular assessment of polymorphism among local Jordanian genotypes of the common fig (Ficus carica L.). Sci Hortic 107:347–351
Sadder MT, Alsadon A, Wahb-Allah M (2014) Transcriptomic analysis of tomato lines reveals putative stress-specific biomarkers. Turk J Agric For 38:700–715
Sadder MT, Al-Doss AA (2014) Characterization of dehydrin AhDHN from Mediterranean saltbush (Atriplex halimus). Turk J Biol 38:469–477
Sadder MT, Anwar F, Al-Doss AA (2013) Gene expression and physiological analysis of Atriplex halimus (L.) under salt stress. Aust J Crop Sci 7:112–118
Sanyal SK, Rao S, Mishra LK, Sharma M, Pandey GK (2016) Plant stress responses mediated by CBL–CIPK phosphorylation network. In: The enzymes, vol 40. Academic Press, pp 31–64. https://doi.org/10.1016/bs.enz.2016.08.002
Sarkar T, Thankappan R, Mishra GP, Nawade BD (2019) Advances in the development and use of DREB for improved abiotic stress tolerance in transgenic crop plants. Physiol Mol Biol Plant 25:1323
Seki M, Narusaka M, Ishida J et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Shi XP, Ren JJ, Yu Q, Zhou SM, Ren QP, Kong LJ, Wang XL (2018) Overexpression of SDH confers tolerance to salt and osmotic stress, but decreases ABA sensitivity in Arabidopsis. Plant Biol 20:327–337
Shirbani S, Haghighi JAP, Jafari M, Davarynejad GH (2013) Physiological and biochemical responses of four edible fig cultivars to water stress condition. Sch J Agric Sci 3:473–479
Siddikee MA, Glick BR, Chauhan PS, Yim WJ, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol Biochem 49:427–434
Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio/Tech 14:407–426
Steppuhn H, Genuchten MT, Grieve CM (2005) Root zone Salinity. Crop Sci 45:221–232
Tamura T, Asakura T, Uemura T, Ueda T, Terauchi K, Misaka T, Abe K (2008) Signal peptide peptidase and its homologs in Arabidopsis thaliana–plant tissue-specific expression and distinct subcellular localization. FEBS J 275:34–43
Usai G, Mascagni F, Giordani T, Vangelisti A, Bosi E, Zuccolo A, Ceccarelli M, King R, Hassani-Pak K, Zambrano LS, Cavallini A, Natali L (2020) Epigenetic patterns within the haplotype phased fig (Ficus carica L.) genome. Plant J 102(3):600–614.
Vangelisti A, Zambrano LS, Caruso G, et al. (2019) How an ancient, salt-tolerant fruit crop, Ficus carica L., copes with salinity: a transcriptome analysis. Sci Rep 9:2561.
Xu C, Tang X, Shao H, Wang H (2016) Salinity tolerance mechanism of economic halophytes from physiological to molecular hierarchy for improving food quality. Curr Genomics 17:207–214
Yamaki S (2010) Metabolism and accumulation of sugars translocated to fruit and their regulation. J J Soc Hortic Sci 79:1–15
Yang Z, Wang C, Xue Y, Liu X, Chen S, Song C, Yang Y, Guo Y (2019) Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10:1199
Zambrano LS, Usai G, Vangelisti A et al (2017) Cultivar-specific transcriptome prediction and annotation in Ficus carica L. Genom Data 13:64–66
Zhu S, Zhou X, Wu X, Jiang Z (2013) Structure and function of the cbl–cipk Ca 2+-decoding system in plant calcium signaling. Plant Mol Biol Rep 31:1193–1202
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The project was funded from Deanship of Scientific Research (Number 1781), University of Jordan, Jordan.
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Supplementary Information
12298_2020_921_MOESM1_ESM.tif
Supplementary Fig. 1 Phylogeny of FcSPPL2B and plants homologs based on parsimony method. Accession numbers are indicated to the left of scientific names. Branching points show bootstrap values. (TIFF 398 kb)
12298_2020_921_MOESM2_ESM.tif
Supplementary Fig. 2 Phylogeny of FcDREB and plants homologs based on parsimony method. Accession numbers are indicated to the left of scientific names. Branching points show bootstrap values. (DOCX 383 kb)
12298_2020_921_MOESM3_ESM.tif
Supplementary Fig. 3 Phylogeny of FcCIPK11 and plants homologs based on parsimony method. Accession numbers are indicated to the left of scientific names. Branching points show bootstrap values. (DOCX 391 kb)
12298_2020_921_MOESM4_ESM.tif
Supplementary Fig. 4 Phylogeny of FcSORD and plants homologs based on parsimony method. Accession numbers are indicated to the left of scientific names. Branching points show bootstrap values. (DOCX 381 kb)
12298_2020_921_MOESM5_ESM.tif
Supplementary Fig. 5 Phylogeny of FcDHN and plants homologs based on parsimony method. Accession numbers are indicated to the left of scientific names. Branching points show bootstrap values. (DOCX 388 kb)
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Sadder, M.T., Alshomali, I., Ateyyeh, A. et al. Physiological and molecular responses for long term salinity stress in common fig (Ficus carica L.). Physiol Mol Biol Plants 27, 107–117 (2021). https://doi.org/10.1007/s12298-020-00921-z
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DOI: https://doi.org/10.1007/s12298-020-00921-z