Abstract
The photosynthetic organs of the barley spike (lemma, palea, and awn) are considered resistant to drought. However, there is little information about gene expression in the spike organs under drought conditions. We compared response of the transcriptome of the lemma, palea, awn, and seed to drought stress using the Barley1 Genome Array. Barley plants were exposed to drought treatment for 4 days at the grain-filling stage by withholding water. At the end of the stress, relative water content of the lemma, palea, and awn dropped from 85% to 60%. Nevertheless, the water content of the seed only decreased from 89% to 81%. Transcript abundance followed the water status of the spike organs; the awn had more drought-regulated genes followed by lemma and palea, and the seed showed very little change in gene expression. Despite expressing more drought-associated genes, many genes for amino acid, amino acid derivative, and carbohydrate metabolism, as well as for photosynthesis, respiration, and stress response, were down-regulated in the awn compared with the lemma, palea, and seed. This suggests that the lemma and the palea are more resistant to drought stress compared with the awn.
References
Abebe T, Skadsen RW, Kaeppler HF (2004) Cloning and identification of highly expressed genes in barley lemma and palea. Crop Sci 44:942–950
Abebe T, Wise RP, Skadsen RW (2009) Comparative transcriptional profiling established the awn as the major photosynthetic organ of the barley spike while the lemma and the palea primarily protect the seed. Plant Genome (in press)
Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390
Araus JL, Brown HR, Febrero A, Bort J, Serret MD (1993) Ear photosynthesis, carbon isotope discrimination and the contribution of respiratory CO2 to differences in grain mass in durum wheat. Plant Cell Environ 16:383–392
Bass HW, Krawetz JE, O'Brian GR, Zinselmeier C, Habben JE, Boston RS (2004) Maize ribosome-inactivating proteins (RIPs) with distinct expression patterns have similar requirements for proenzyme activation. J Exp Bot 55:2219–2233
Blum A (1985) Photosynthesis and transpiration in leaves and ears of wheat and barley varieties. J Exp Bot 36:432–440
Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
Boyer JS, Westgate ME (2004) Grain yields with limited water. J Exp Bot 55:2385–2394
Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1158–1203
Cameron DK, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140:176–183
Caspi R, Foerster H, Fulcher CA, Kaipa P, Krummenacker M, Latendresse M, Paley S, Rhee SY, Rhee SY, Shearer AG, Tissier C, Zhang P, Karp PD (2008) MetaCyc: a multiorganism database of metabolic pathways and enzymes. Nucleic Acids Res 34:D511–D516
Castrillo M, Fernandez D, Calcagno AM, Trujillo I, Guenni L (2001) Responses of ribulose-1, 5-bisphosphate carboxylase, protein content, and stomatal conductance to water deficit in maize, tomato, and bean. Photosynthetica 39:221–226
Chaves MM, Flexas J, Pinheiro C (2007) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
Chen H, McCaig BC, Melotto M, He SY, Howe GA (2004) Regulation of plant arginase by wounding, jasmonate and the phytotoxin coronatine. J Biol Chem 279:45998–46007
Chirgwin JM, Prybyla A, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochem 18:5294–5299
Close TJ, Wanamaker S, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP (2004) A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol 134:960–968
Danuta C, Romualda K, Agnieszka C, Marta J (2008) Influence of long-term drought stress on osmolyte accumulation in sugar beet (Beta vulgaris L.) plants. Acta Physiol Plant 30:679–687
Duffus CM, Cochrane MP (1993) Formation of the barley grain—morphology, physiology, and biochemistry. In: MacGregor AW, Bhatty RS (eds) Barley: chemistry and technology. American Association of Cereal Chemists, St. Paul, pp 31–72
Fait A, Yellin A, Fromm H (2004) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415–420
Fan L, Linker R, Gepstein S, Tanimoto E, Yamamoto R, Neumann PM (2006) Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lignin metabolism and progressive stelar accumulation of wall phenolics. Plant Physiol 140:603–612
Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189
Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364
Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan Y-F, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of alternative oxidase1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147:595–610
Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
Guo P, Baum M, Grando S, Ceccarelli S, Bai G, Li R, von Korff M, Varshney RK, Graner A, Valkoun J (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot. doi:10.1093/jxb/erp194
Ho LHM, Giraud E, Uggalla V, Lister R, Clifton R, Glen A, Thirkettle-Watts D, Van Aken O, Whelan J (2008) Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol 147:1858–1873
Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438
Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Abidopsis thaliana. Plant Cell Physiol 45:712–722
Kishor KPB, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of ∆-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394
Nettleton D (2006) A discussion of statistical methods for design and analysis of microarray experiments for plant scientists. Plant Cell 18:2112–2121
Ober E, Sharp RE (2007) Regulation of root growth responses to water deficit. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, The Netherlands, pp 33–53
Ober ES, Setter TL, Madison JT, Thompson JF, Shapiro PS (1991) Influence of water deficit on maize endosperm development: enzyme activities and RNA transcripts of starch and zein synthesis, abscisic acid, and cell division. Plant Physiol 97:154–164
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annual Rev Plant Biol 59:417–441
Rachmilevitch S, DaCosta M, Huang B (2006) Physiological and biochemical indicators for stress tolerance. In: Huang B (ed) Plant–environment interactions, 3rd edn. CRC Press, Boca Raton, pp 321–355
Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271
Saini HS, Westgate ME (2000) Reproductive development in grain crops during drought. Adv Agron 68:59–96
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CΤ method. Nature protocols 3:1101–1108
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (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
Setter TL, Flannigan BA, Melkonian J (2001) Loss of kernel set due to water deficit and shade in maize: carbohydrate supplies, abscisic acid, and cytokinins. Crop Sci 41:1530–1540
Shen L, Gong J, Caldo RA, Nettleton D, Cook D, Wise RP, Dickerson JA (2005) BarleyBase—an expression profiling database for plant genomics. Nucleic Acids Res 33:D614–D618
Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotechnol 9:214–219
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440–9445
Talame V, Ozturk NZ, Bohnert HJ, Tuberosa R (2006) Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J Exp Bot 58:229–240
Tambussi EA, Bort J, Guiamet JJ, Nogúes S, Araus JL (2007) The photosynthetic role of ears in C3 cereals: metabolism, water use efficiency and contribution to grain yield. Crit Rev Plant Sci 26:1–16
Tassonia A, Franceschettia M, Bagn N (2008) Polyamines and salt stress response and tolerance in Arabidopsis thaliana flowers. Plant Physiol Biochem 46:607–613
Tommasini L, Svensson JT, Rodriguez EM, Wahid A, Malatrasi M, Kato K, Wanamaker S, Resnik J, Close TJ (2008) Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Funct Integr Genomics 8:387–405
Umbach AL, Fiorani F, Siedow JN (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissues. Plant Physiol 139:1806–1820
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139:822–835
Westgate ME (1994) Water status and development of the maize endosperm and embryo during drought. Crop Sci 34:76–83
Yang J, Zhang J, Liu K, Wang Z, Liu L (2007) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58:1545–1555
Yeats TH, Rose JKC (2008) The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Sci 17:191–198
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421
Zinselmeier C, Sun Y, Helentjaris T, Beatty M, Yang S, Smith H, Habben J (2002) The use of gene expression profiling to dissect the stress sensitivity of reproductive development in maize. Field Crops Res 75:111–121
Acknowledgments
We thank Diveena Vijeyandran, Aaron Walck, Ng Eng Hwa, Emily Jackson, and Justin Wilkins for their help on sample collection and RNA extraction and Matthew Moscou for initial analysis of the data set. We are grateful to Billie Hemmer and Stephanie Witt for assistance in growing plants. We thank Dr. Tesfaye Mersha for his advice on statistical analysis. This work was supported by the Board of Regents of the State of Iowa and the Office of Sponsored Programs, the Graduate College, the College of Natural Sciences and the Department of Biology of the University of Northern Iowa, Cedar Falls, Iowa. We thank Dr. Ronald W. Skadsen for his valuable comments.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Materials
Below is the link to the electronic supplementary material.
Supplementary Figure S1
Organ-specific expression of drought-regulated genes in the spike (DOC 74 kb)
Supplementary Table S1
Primer sequences for real-time PCR (DOC 76 kb)
Supplementary Table S2
RWC of drought-stressed lemma, palea, awn, and seed of barley (DOC 73 kb)
Supplementary Table S3
Expression profile of genes associated with major GO biological process categories in drought-stressed organs of the barley spike (XLS 205 kb)
Supplementary Table S4
Comparison of gene expression in the spike organs using the Barley1 GeneChip and real-time PCR (DOC 75 kb)
Rights and permissions
About this article
Cite this article
Abebe, T., Melmaiee, K., Berg, V. et al. Drought response in the spikes of barley: gene expression in the lemma, palea, awn, and seed. Funct Integr Genomics 10, 191–205 (2010). https://doi.org/10.1007/s10142-009-0149-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-009-0149-4