Physiological and Transcriptomics Analyses Reveal that Ascophyllum nodosum Extracts Induce Salinity Tolerance in Arabidopsis by Regulating the Expression of Stress Responsive Genes
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Extracts of the brown alga, Ascophyllum nodosum, are widely used as plant biostimulants to improve growth and to impart tolerance against abiotic stresses. However, the molecular mechanisms by which A. nodosum extract (ANE) mediates stress tolerance are still largely unknown. The aim of this study was to study selected anti-stress mechanisms at the transcriptome level. We show that methanolic sub-fractions of ANE improved growth of Arabidopsis thaliana under NaCl stress; biomass increased by approximately 50% under 100 mM and 150 mM NaCl, relative to the control. Bioassay-guided fractionation revealed that the ethyl acetate sub-fraction of ANE (EAA) had the majority of stress alleviating, bioactive components. Microarray analysis showed that EAA elicited substantial changes in the global transcriptome on day 1 and day 5, after treatment. On day one, 184 genes were up-regulated while this number increased to 257 genes on day 5. On the other hand, 91 and 262 genes were down-regulated on day 1 and day 5, respectively. On day 1, 2.2% of the genes altered were abiotic stress regulated and this increased to 6% on day 5. EAA modulate the expression of number of the genes involved in stress responses, carbohydrate metabolism, and phenylpropanoid metabolism. Thus, our results suggested that bioactive components in the ethyl acetate fraction of A. nodosum induced salinity tolerance in A. thaliana by modulating the expression of a plethora of stress-responsive genes, providing a better understanding of the mechanisms through which ANE mediates tolerance by plants to salinity stress.
KeywordsAscophyllum nodosum Arabidopsis Bioactive compounds Salinity stress Organic extracts
Authors are grateful for the valuable suggestions of Dr. Dhirti Battacharya and Emily Mantin for reading the manuscript. The work reported in this paper was partly funded by Atlantic Innovation Fund program of Atlantic Canada Opportunities Agency and Acadian Seaplants Limited.
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Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be considered as a potential conflict of interest. Authors declare no conflict of interest, financial or non-financial.
- Al-Maskri A, Al-Kharusi L, Al-Miqbali H (2010) Effects of salinity stress on growth of lettuce (Lactuca sativa) under closed-recycle nutrient film technique. Int J Agric Biol 12:377–380Google Scholar
- Fan D, Hodges DM, Zhang J, Kirby CW, Ji X, Locke SJ, Critchley AT, Prithiviraj B (2011) Commercial extract of the brown seaweed Ascophyllum nodosum enhances phenolic antioxidant content of spinach (Spinacia oleracea L.) which protects Caenorhabditis elegans against oxidative and thermal stress. Food Chem 124(1):195–202CrossRefGoogle Scholar
- 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 6:9228Google Scholar
- Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. Plant J 9:537–548. https://doi.org/10.1046/j.1365-313X.1996.09040537.x CrossRefPubMedGoogle Scholar
- Jithesh MN, Wally OSD, Manfield I, Critchley AT, Hiltz D, Prithiviraj B (2012) Analysis of seaweed extract-induced transcriptome leads to identification of a negative regulator of salt tolerance in Arabidopsis. Hortic Sci 47:704–709Google Scholar
- Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
- Peng Z, Lu Q, Verma DP (1996) Reciprocal regulation of ∆ 1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol Genet Genomics 253:334–341Google Scholar
- Rayorath P, Jithesh MN, Farid A, Khan W, Palanisamy R, Hankins SD et al (2008) Rapid bioassays to evaluate the plant growth promoting activity of Ascophyllum nodosum (L.) Le Jol. using a model plant, Arabidopsis thaliana (L.) Heynh. J Appl Phycol 20:423–429. https://doi.org/10.1007/s10811-007-9280-6 CrossRefGoogle Scholar
- Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M (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(3):279–292. https://doi.org/10.1046/j.1365-313X.2002.01359.x CrossRefPubMedGoogle Scholar
- Subramanian S, Sangha JS, Gray BA, Singh RP, Hiltz D, Critchley AT et al (2011) Extracts of the marine brown macroalga, Ascophyllum nodosum, induce jasmonic acid dependent systemic resistance in Arabidopsis thaliana. against Pseudomonas syringae pv. tomato DC3000 and Sclerotinia sclerotiorum. Eur J Plant Pathol 131:237–248. https://doi.org/10.1007/s10658-011-9802-6 CrossRefGoogle Scholar
- Szabolcs I (1994) Soils and salinisation. In: Pessarakali M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 3–11Google Scholar
- Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K et al (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709. https://doi.org/10.1104/pp.104.039909 CrossRefPubMedPubMedCentralGoogle Scholar
- Wally OSD, Critchley AT, Hiltz D, Craigie JS, Han X, Zaharia LI et al (2013) Regulation of phytohormone biosynthesis and accumulation in Arabidopsis following treatment with commercial extract from the marine macroalga Ascophyllum nodosum. J Plant Growth Regul 32:324–339. https://doi.org/10.1007/s00344-012-9301-9 CrossRefGoogle Scholar
- Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol 12:188. https://doi.org/10.1186/1471-2229-12-188 CrossRefPubMedPubMedCentralGoogle Scholar