Share This Article:

Transcriptome Analysis of Drought Induced Stress in Chenopodium quinoa

Full-Text HTML Download Download as PDF (Size:783KB) PP. 338-357
DOI: 10.4236/ajps.2014.53047    5,507 Downloads   8,959 Views   Citations

ABSTRACT

Quinoa (Chenopodium quinoa Willd.) is a halophytic, allotetraploid grain crop of the Amaranthaceae family with impressive drought tolerance, nutritional content and an increasing worldwide market. Here we report the results of an RNA-seq transcriptome analysis of Chenopodium quinoa using four water treatments (field capacity to drought) on the varietiesIngapirca (representing valley ecotypes) and Ollague (representing Altiplano Salares ecotypes). Physiological results, including growth rate, photosynthetic rate, stomatal conductance, and stem water potential, support the earlier findings that the Altiplano Salares ecotypes display greater tolerance to drought-like stress conditions than the valley ecotypes. cDNA libraries from root tissue samples for each variety × treatment combination were sequenced using Illumina Hi-Seq technology in an RNA-seq experiment. De novo assembly of the transcriptome generated 20,337 unique transcripts. Gene expression analysis of the RNA-seq data identified 462 putative gene products that showed differential expression based on treatment, and 27 putative gene products differentially expressed based on variety × treatment, including significant expression differences in root tissue in response to increasing water stress. BLAST searches and gene ontology analysis show an overlap between drought tolerance stress and other abiotic stress mechanisms.

Cite this paper

J. Raney, D. Reynolds, D. Elzinga, J. Page, J. A. Udall, E. Jellen, A. Bonfacio, D. Fairbanks and P. Maughan, "Transcriptome Analysis of Drought Induced Stress in Chenopodium quinoa," American Journal of Plant Sciences, Vol. 5 No. 3, 2014, pp. 338-357. doi: 10.4236/ajps.2014.53047.

References

[1] H. W. Koyro and S. S. Eisa, “Effect of Salinity on Composition, Viability and Germination of Seeds of Chenopodium Quinoa Willd,” Plant Soil, Vol. 302, No. 1-2, 2008, pp. 79-90.
http://dx.doi.org/10.1007/s11104-007-9457-4
[2] S. E. Jacobsen, “The Worldwide Potential for Quinoa (Chenopodium Quinoa Willd),” Food Reviews International, Vol. 19, No. 1-2, 2003, pp. 167-177.
http://dx.doi.org/10.1081/FRI-120018883
[3] M. Tapia, H. Gandarillas, S. Alandia, A. Cardozo, A. Mujica, R. Ortiz, et al., “Quinoa y Kañahua: Cultivos Andinos,” CIID-IICA, Bogotá, 1979.
[4] S. G. Wood, L. D. Lawson, D. J. Fairbanks, L. R. Robison and W. R. Andersen, “Seed Lipid Content and Fatty Acid Composition of Three Quinoa Cultivars,” Journal of Food Composition and Analysis, Vol. 6, No. 1, 1993, pp. 41-44.
[5] P. M. Ruas, A. Bonifacio, C. F. Ruas, D. J. Fairbanks and W. R. Andersen, “Genetic Relationship among 19 Accessions of Six Species of Chenopodium L., by Random Amplified Polymorphic DNA Fragments (RAPD),” Euphytica, Vol. 105, No. 1999, pp. 25-32.
[6] J. Ruales and B. M. Nair, “Content of Fat, Vitamins and Minerals in Quinoa (Chenopodium Quinoa, Willd) Seeds,” Food Chemistry, Vol. 48, No. 2, 1993, pp. 131-136.
[7] United Nations, “The Food and Agriculture Organization: International Year of Quinoa: 2013,” United Nations General Assembly 66th Session, 2011.
http://www.un.org/ga/search/view_doc.asp?symbol=A/C.2/66/L.19
[8] S. A. Valencia-Chamorro, “Quinoa,” In: B. Caballero, Ed., Encyclopedia of Food Science and Nutrition, Academic Press, Waltham, 2003, pp. 4895-4902.
http://dx.doi.org/10.1016/B0-12-227055-X/00995-0
[9] J. J. Vacher, “Responses of Two Main Andean Crops, Quinoa (Chenopodium quinoa Willd.) and Papa Amarga (Solanum juzepczukii Buk.) to Drought on the Bolivian Altiplano: Significance of Local Adaptation,” Agriculture, Ecosystems & Environment, Vol. 68, No. 1-2, 1998, pp. 99-108.
http://dx.doi.org/10.1016/S0167-8809(97)00140-0
[10] F. E. Prado, C. Boero, M. Gallardo and J. A. Gonzalez, “Effect of Nacl on Germination, Growth, and Soluble Sugar Content in Chenopodium quinoa Willd. Seeds,” Botanical Bulletin of Academia Sinica, Vol. 41, No. 1, 2000, pp. 27-34.
[11] S. E. Jacobsen, C. Monteros, L. J. Corcuera, L. A. Bravo, J. L. Christiansen and A. Mujica, “Frost Resistance Mechanisms in Quinoa (Chenopodium quinoa Willd.),” European Journal of Agronomy, Vol. 26, No. 4, 2007, pp. 471-475. http://dx.doi.org/10.1016/j.eja.2007.01.006
[12] C. J. Risi and N. W. Galwey, “The Chenopodium Grains of the Andes: Inca Crops for Modern Agriculture,” Advances in Applied Biology, Vol. 10, 1984, pp. 145-216.
[13] H. Gandarillas, “Quinoa y Kañiwa: Cultivos Andinos. Bogotá,” Instituto Interamericano de Ciencias Agrícolas, Colombia, 1979.
[14] J. S. Boyer, “Plant Productivity and Environment,” Science, Vol. 218, No. 4571, 1982, pp. 443-448.
http://dx.doi.org/10.1126/science.218.4571.443
[15] D. Bartels and D. Nelson, “Approaches to Improve Stress Tolerance Using Molecular Genetics,” Plant, Cell & Environment, Vol. 17, No. 5, 1994, pp. 659-667.
http://dx.doi.org/10.1111/j.1365-3040.1994.tb00157.x
[16] E. R. Cook, R. Seager, M. A. Cane and D. W. Stahle, “North American Drought: Reconstructions, Causes, and Consequences,” Earth-Science Reviews, Vol. 81, No. 1-2, 2007, pp. 93-134.
http://dx.doi.org/10.1016/j.earscirev.2006.12.002
[17] US, “Drought 2012: Farm and Food Impacts,”
http://www.ers.usda.gov/newsroom/us-drought-2012-farm-and-food-impacts.aspx
[18] A. Lowry and R. Nixon, “Severe Drought Seen as Driving Cost of Food up,” New York Times, 2012.
http://www.nytimes.com/2012/07/26/business/food-prices-to-rise-in-wake-of-severe-drought.html
[19] S. E. Jacobsen, “The Worldwide Potential for Quinoa (Chenopodium quinoa Willd.),” Food Reviews International, Vol. 19, No. 1-2, 2003, pp. 167-177.
[20] B. R. Trognitz, “Prospects of Breeding Quinoa for Tolerance to Abiotic Stress,” Food Reviews International, Vol. 19, No. 1-2, 2003, pp. 129-137.
[21] J. A. Kreps, Y. Wu, H.-S. Chang, T. Zhu, X. Wang and J. F. Harper, “Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress,” Plant Physiology, Vol. 130, No. 4, 2002, pp. 2129-2141.
http://dx.doi.org/10.1104/pp.008532
[22] R. Kawaguchi, T. Girke, E. A. Bray and J. Bailey-Serres, “Differential mRNA Translation Contributes to Gene Regulation under Non-Stress and Dehydration Stress Conditions in Arabidopsis Thaliana,” Plant Journal, Vol. 38, No. 5, 2004, pp. 823-839.
http://dx.doi.org/10.1111/j.1365-313X.2004.02090.x
[23] J. G. Dubouzet, Y. Sakuma, Y. Ito, M. Kasuga, E. G. Dubouzet, S. Miura, et al., “Osdreb Genes in Rice, Oryza sativa L., Encode Transcription Activators That Function in Drought-, High-Salt- and Cold-Responsive Gene Expression,” Plant Journal, Vol. 33, No. 4, 2003, pp. 751-763. http://dx.doi.org/10.1046/j.1365-313X.2003.01661.x
[24] M. Gorantla, P. R. Babu, V. B. R. Lachagari, F. A. Feltus, A. H. Paterson and A. R. Reddy, “Functional Genomics of Drought Stress Response in Rice: Transcript Mapping of Annotated Unigenes of an Indica Rice (Oryza sativa L. Cv. Nagina 22),” Current Science India, Vol. 89, No. 3, 2005, pp. 496-514.
[25] C. D. Buchanan, S. Y. Lim, R. A. Salzman, L. Kagiampakis, D. T. Morishige, B. D. Weers, et al., “Sorghum Bicolor’s Transcriptome Response to Dehydration, High Salinity and ABA,” Plant Molecular Biology, Vol. 58, No. 5, 2005, pp. 699-720.
http://dx.doi.org/10.1007/s11103-005-7876-2
[26] P. J. Maughan, T. B. Turner, C. E. Coleman, D. B. Elzinga, E. N. Jellen, J. A. Morales, et al., “Characterization of Salt Overly Sensitive 1 (SOS1) Gene Homoeologs in Quinoa (Chenopodium quinoa Wilid.),” Genome, Vol. 52, No. 7, 2009, pp. 647-657.
http://dx.doi.org/10.1139/G09-041
[27] A. J. Morales, P. Bajgain, Z. Garver, P. J. Maughan and J. A. Udall, “Evaluation of the Physiological Responses of Chenopodium quinoa to Salt Stress,” International Journal of Plant Physiology and Biochemistry, Vol. 3, No. 13, 2011, pp. 219-232.
[28] S. L. Mason, M. R. Stevens, E. N. Jellen, A. Bonifacio, D. J. Fairbanks, C. E. Coleman, et al., “Development and Use of Microsatellite Markers for Germplasm Characterization in Quinoa (Chenopodium quinoa Willd.),” Crop Science, Vol. 45, No. 4, 2005, pp. 1618-1630.
http://dx.doi.org/10.2135/cropsci2004.0295
[29] M. Nagata and I. Yamashita, “Simple Method for Simultaneous Determination of Chlorophyll and Carotenoids in Tomato Fruit,” Japan Society of Nutrition and Food Science, Vol. 39, No. 10, 1992, pp. 925-928.
[30] R. Development Core Team, “R: A Language and Environment for Statistical Computing,” Version 2.15.1, 2012.
[31] H. J. Earl, “A Precise Gravimetric Method for Simulating Drought Stress in Pot Experiments,” Crop Science, Vol. 43, No. 5, 2003, pp. 1868-1873.
http://dx.doi.org/10.2135/cropsci2003.1868
[32] M. G. Grabherr, B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson, I. Amit, et al., “Full-Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome,” Nature Biotechnology, Vol. 29, No. 7, 2011, pp. 644-652. http://dx.doi.org/10.1038/nbt.1883
[33] T. D. Wu and S. Nacu, “Fast and Snp-Tolerant Detection of Complex Variants and Splicing in Short Reads,” Bioinformatics, Vol. 26, No. 7, 2010, pp. 873-881.
http://dx.doi.org/10.1093/bioinformatics/btq057
[34] A. Mortazavi, B. A. Williams, K. Mccue, L. Schaeffer and B. Wold, “Mapping and Quantifying Mammalian Transcriptomes by RNA-Seq,” Nature Methods, Vol. 5, No. 7, 2008, pp. 621-628.
http://dx.doi.org/10.1038/nmeth.1226
[35] M. D. Robinson, D. J. McCarthy and G. K. Smyth, “Edger: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data,” Bioinformatics, Vol. 26, No. 1, 2010, pp. 139-140.
http://dx.doi.org/10.1093/bioinformatics/btp616
[36] Y. Benjamini and Y. Hochberg, “Controlling the False Discovery Rate—A Practical and Powerful Approach to Multiple Testing,” Journals of the Royal Statistical Society, Vol. 57, No. 1, 1995, pp. 289-300.
[37] S. F. Altschul, T. L. Madden, A. A. Schaffer, J. H. Zhang, Z. Zhang, W. Miller, et al., “Gapped Blast and Psi-Blast: A New Generation of Protein Database Search Programs,” Nucleic Acids Research, Vol. 25, No. 17, 1997, pp. 3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389
[38] S. Gotz, J. M. Garcia-Gomez, J. Terol, T. D. Williams, S. H. Nagaraj, M. J. Nueda, et al., “High-Throughput Functional Annotation and Data Mining with the Blast2Go Suite,” Nucleic Acids Research, Vol. 36, No. 10, 2008, pp. 3420-3435.
http://dx.doi.org/10.1093/nar/gkn176
[39] N. Bluthgen, K. Brand, B. Cajavec, M. Swat, H. Herzel and D. Beule, “Biological Profiling of Gene Groups Utilizing Gene Ontology,” Genome Informatics International Conference on Genome Informatics, Vol. 16, No. 1, 2005, pp. 106-115.
[40] H. Ogata, S. Goto, K. Sato, W. Fujibuchi, H. Bono and M. Kanehisa, “Kegg: Kyoto Encyclopedia of Genes and Genomes,” Nucleic Acids Research, Vol. 27, No. 1, 1999, pp. 29-34. http://dx.doi.org/10.1093/nar/27.1.29
[41] X. Chone, C. van Leeuwen, D. Dubourdieu and J. P. Gaudillere, “Stem Water Potential Is a Sensitive Indicator of Grapevine Water Status,” Annals of Botany—London, Vol. 87, No. 4, 2001, pp. 477-483.
http://dx.doi.org/10.1006/anbo.2000.1361
[42] D. Reynolds, “Genetic Dissection of Triterpenoid Saponin Production in Chenopodium quinoa Using Microarray Analysis,” M.S. Thesis, Brigham Young University, Provo, 2009.
[43] S. E. Jacobsen, F. L. Liu and C. R. Jensen, “Does Root-Sourced Aba Play a Role for Regulation of Stomata under Drought in Quinoa (Chenopodium quinoa Willd.),” Scientia Horticulturae—Amsterdam, Vol. 122, No. 2, 2009, pp. 281-287. http://dx.doi.org/10.1016/j.scienta.2009.05.019
[44] C. R. Jensen, S. E. Jacobsen, M. N. Andersen, N. Nunez, S. D. Andersen, L. Rasmussen, et al., “Leaf Gas Exchange and Water Relation Characteristics of Field Quinoa (Chenopodium quinoa Willd.) during Soil Drying,” European Journal of Agronomy, Vol. 13, No. 1, 2000, pp. 11-25. http://dx.doi.org/10.1016/S1161-0301(00)00055-1
[45] J. A. Gonzalez, M. Bruno, M. Valoy and F. E. Prado, “Genotypic Variation of Gas Exchange Parameters and Leaf Stable Carbon and Nitrogen Isotopes in Ten Quinoa Cultivars Grown under Drought,” Journal of Agronomy and Crop Science, Vol. 197, No. 2, 2011, pp. 81-93.
http://dx.doi.org/10.1111/j.1439-037X.2010.00446.x
[46] M. E. Tapia, “Origen, Distribución Geográfica y Sistemas de Producción de la Quinua,” In: PISCA-UNTA-IBTAIICA-CIID, Ed., Reunión Sobre Genética Y Fitomejoramiento de la Quinua, Puno, 1980.
[47] J. C. Vera, C. W. Wheat, H. W. Fescemyer, M. J. Frilander, D. L. Crawford, I. Hanski, et al., “Rapid Transcriptome Characterization for a Nonmodel Organism Using 454 Pyrosequencing,” Molecular Ecology, Vol. 17, No. 7, 2008, pp. 1636-1647.
http://dx.doi.org/10.1111/j.1365-294X.2008.03666.x
[48] R. Ekblom and J. Galindo, “Applications of Next Generation Sequencing in Molecular Ecology of Non-Model Organisms,” Heredity, Vol. 107, No. 1, 2011, pp. 1-15.
http://dx.doi.org/10.1038/hdy.2010.152
[49] M. L. Metzker, “Sequencing Technologies—The Next Generation,” Nature Reviews Genetics, Vol. 11, No. 1, 2010, pp. 31-46.
http://dx.doi.org/10.1038/nrg2626
[50] K. Shinozaki and K. Yamaguchi-Shinozaki, “Gene Networks Involved in Drought Stress Response and Tolerance,” Journal of Experimental Botany, Vol. 58, No. 2, 2007, pp. 221-227. http://dx.doi.org/10.1093/jxb/erl164
[51] K. Shinozaki, K. Yamaguchi-Shinozaki and M. Seki, “Regulatory Network of Gene Expression in the Drought and Cold Stress Responses,” Current Opinion in Plant Biology, Vol. 6, No. 5, 2003, pp. 410-417.
http://dx.doi.org/10.1016/S1369-5266(03)00092-X
[52] I. Hernandez, L. Alegre and S. Munne-Bosch, “Drought-Induced Changes in Flavonoids and Other Low Molecular Weight Antioxidants in Cistus clusii Grown under Mediterranean Field Conditions,” Tree Physiology, Vol. 24, No. 11, 2004, pp. 1303-1311.
http://dx.doi.org/10.1093/treephys/24.11.1303
[53] C. Yunta, M. Martinez-Ripoll and A. Albert, “Snrk2.6/ Ost1 from Arabidopsis Thaliana: Cloning, Expression, Purification, Crystallization and Preliminary X-Ray Analysis of K50n and D160a Mutants,” Acta Crystallographica Section F, Structural Biology and Crystallization Communications, Vol. 67, No. 3, 2011, pp. 364-368.
http://dx.doi.org/10.1107/S1744309110053807
[54] G. Lopez-Frias, L. M. Martinez, G. Ponce, G. I. Cassab and J. Nieto-Sotelo, “Role of Hsp101 in the Stimulation of Nodal Root Development from the Coleoptilar Node by Light and Temperature in Maize (Zea mays L.) Seedlings,” Journal of Experimental Botany, Vol. 62, No. 13, 2011, pp. 4661-4673.
http://dx.doi.org/10.1093/jxb/err186
[55] H. Yamamoto, N. Katano, A. Ooi and K. Inoue, “Secologanin Synthase Which Catalyzes the Oxidative Cleavage of Loganin into Secologanin Is a Cytochrome P450,” Phytochemistry, Vol. 53, No. 1, 2000, pp. 7-12.
http://dx.doi.org/10.1016/S0031-9422(99)00471-9
[56] J. L. Martindale and N. J. Holbrook, “Cellular Response to Oxidative Stress: Signaling for Suicide and Survival,” Journal of Cellular Physiology, Vol. 192, No. 1, 2002, pp. 1-15. http://dx.doi.org/10.1002/jcp.10119
[57] S. Kitajima and F. Sato, “Plant Pathogenesis-Related Proteins: Molecular Mechanisms of Gene Expression and Protein Function,” The Journal of Biochemistry—Tokyo, Vol. 125, No. 1, 1999, pp. 1-8.
http://dx.doi.org/10.1093/oxfordjournals.jbchem.a022244
[58] R. Przymusinski, R. Rucinska and E. A. Gwozdz, “Increased Accumulation of Pathogenesis-Related Proteins in Response of Lupine Roots to Various Abiotic Stresses,” Environmental and Experimental Botany, Vol. 52, No. 1, 2004, pp. 53-61.
http://dx.doi.org/10.1016/j.envexpbot.2004.01.006

  
comments powered by Disqus

Copyright © 2017 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.