Abstract
Smoke from burning vegetation is widely recognised as a germination cue for seed germination and recent reports suggest that smoke treatments can improve seedling vigour also. We investigated the effect of smoke-water on seedling vigour and changes of the global transcriptome in the early post-germination phase in maize. Application of smoke-water improved the germination characteristics and seedling vigour. The transcriptional response of embryos and emerging radicles 24 and 48 h after the onset of smoke treatment was investigated. The microarray study revealed a number of smoke-responsive genes amongst which stress- and abscisic acid (ABA)-related genes were over-represented. The global promoter analysis of the smoke-responsive genes revealed a tight correlation with the results obtained from Gene Ontology annotations. This concerted over-expression shows that smoke treatment induces stress and ABA-related responses in the early post-germination phase which leads to better adaptation to environmental stress factors occurring during germination, eventually resulting in greater seedling vigour.
Similar content being viewed by others
References
Adkins SW, Peters NCB (2001) Smoke derived from burnt vegetation stimulates germination of arable weeds. Seed Sci Res 11:213–222
Aguilar ML, Espadas FL, Coello J, Maust BE, Trejo C, Robert ML, Santamaria JM (2000) The role of abscisic acid in controlling leaf water loss, survival and growth of micropropagated Tagetes erecta plants when transferred directly to the field. J Exp Bot 51:1861–1866
Albacete AA, Martínez-Andújar C, Pascual JA, Acosta M, Pérez-Alfocea F (2008) Increasing vegetative growth, yield and seed quantity in tomato by inducing plant vigour at the earliest seedling stage. Acta Hort 782:265–272
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT et al (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Gen 25:25–29
Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56:2071–2083
Baxter BJM, Van Staden J (1994) Plant-derived smoke: an effective seed pre-treatment. Plant Growth Regul 14:279–282
Baxter BJM, Van Staden J, Granger JE, Brown NAC (1994) Plant-derived smoke and smoke extracts stimulate seed germination of the fire-climax grass Themeda triandra Forssk. Env Exp Bot 34:217–223
Bell DT (1999) Turner review no. 1—the process of germination in Australian species. Aust J Bot 47:475–517
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Brown NAC (1993) Promotion of germination of fynbos seeds by plant-derived smoke. New Phytol 123:575–583
Brown NAC, Van Staden J, Daws MI, Johnson T (2003) Patterns in the seed germination response to smoke in plants from the Cape Floristic Region, South Africa. S Afr J Bot 69:514–525
Castillo-Davis CI, Hartl DL (2003) GeneMerge: post-genomic analysis, data mining, and hypothesis testing. Bioinformatics 19:891–892
Chandler PM, Robertson M (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45:113–141
Daws MI, Davies J, Pritchard HW, Brown NAC, Van Staden J (2007) Butenolide from plant-derived smoke enhances germination and seedling growth of arable weed species. Plant Growth Regul 51:73–82
De Smet I, Zhang H, Inzé D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–459
Dhindwal AS, Lather BPS, Singh J (1991) Efficacy of seed treatment on germination, seedling emergence and vigour of cotton (Gossypium hirsutum) genotypes. Seed Res 19:59–61
Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822
Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977
Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit D, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80
Hall HK, McWha JA (1981) Effects of abscisic acid on growth of wheat (Triticum aestivum L.). Ann Bot 47:427–433
Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008) Post-genomics dissection of seed dormancy and germination. Trends Plant Sci 13:7–13
Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264
Keeley JE, Fotheringham CJ (1998) Smoke-induced seed germination in California chaparral. Ecology 79:2320–2336
Khajeh-Hosseini M, Powell AA, Bingham IJ (2003) The interaction between salinity stress and seed vigour during germination of soyabean seeds. Seed Sci Technol 31:715–725
Kirch HH, Schlingensiepen S, Kotchoni S, Sunkar R, Bartels D (2005) Detailed expression analysis of selected genes of the aldehyde dehydrogenase (ALDH) gene superfamily in Arabidopsis thaliana. Plant Mol Biol 57:315–332
Light ME, Gardner MJ, Jager AK, van Staden J (2002) Dual regulation of seed germination by smoke solutions. Plant Growth Regul 37:135–141
Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328
Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S et al (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34:D108–D110
McLaren JS (2005) Crop biotechnology provides an opportunity to develop a sustainable future. Trends Biotechnol 23:339–342
Modi AT (2002) Indigenous storage method enhances seed vigour of traditional maize. S Afr J Sci 98:138–139
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148
Pritchard SL, Charlton WL, Baker A, Graham IA (2002) Germination and storage reserve mobilization are regulated independently in Arabidopsis. Plant J 31:639–647
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0, URL http://www.R-project.org
Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134:1598–1613
Rajjou L, Huguet R, Robin C, Belghazi M, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923
Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16:276–277
Ritchie ME, Diyagama D, Neilson J, van Laar R, Dobrovic A, Holloway A, Smyth GK (2006) Empirical array quality weights in the analysis of microarray data. BMC Bioinformatics 7:261
Roche S, Dixon KW, Pate JS (1997) Seed ageing and smoke: partner cues in the amelioration of seed dormancy in selected Australian native species. Aust J Bot 45:783–815
Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic expression by abscisic acid signaling. Plant J 26:421–433
Smith-Espinoza CJ, Phillips JR, Salamini F, Bartels D (2005) Identification of further Craterostigma plantagineum cdt mutants affected in abscisic acid mediated desiccation tolerance. Mol Genet Genomics 274(4):364–372
Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 31:1–25
Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, USA, pp 397–420
Soeda Y, Konings MC, Vorst O, van Houwelingen AM, Stoopen GM, Maliepaard CA, Kodde J, Bino RJ, Groot SPC, van der Geest AHM (2005) Gene expression programs during Brassica oleracea seed maturation, osmopriming, and germination are indicators of progression of the germination process and the stress tolerance level. Plant Physiol 137:354–368
Sparg SG, Kulkarni MG, Light ME, Van Staden J (2005) Improving seedling vigour of indigenous medicinal plants with smoke. Bioresource Technol 96:1323–1330
Sparg SG, Kulkarni MG, Van Staden J (2006) Aerosol smoke and smoke water stimulation of seedling vigour of a commercial maize cultivar. Crop Sci 46:1336–1340
Van Staden J, Brown NAC, Jäger AK, Johnson TA (2000) Smoke as a germination cue. Plant Spec Biol 15:167–178
Van Staden J, Jäger AK, Light ME, Burger BV (2004) Isolation of the major germination cue from plant-derived smoke. S Afr J Bot 70:654–659
Wang H, Darla R, Georges F, Loewen M, Cuter AJ (1995) Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol Biol 28:605–617
Yang YH, Thorne NP (2003) Normalization for two-color cDNA microarray data. In: Goldstein DR (ed) Science and statistics: a Festschrift for Terry Speed, vol. 40. IMS Lecture Notes—Monograph Series. IMS, Beachwood, OH, pp 403–418
Yang YH, Dudoits S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Acknowledgments
This work was supported by the Generation Challenge Program (GCP), the Hungarian–South African Intergovernmental S&T Cooperation Programme, the Hungarian Scientific Research Fund (OTKA—F16066), the Baross Gábor Projekt and the National Research Foundation, Pretoria, South Africa. Thanks are due to Ferenc Marincs for his kind advices.
Author information
Authors and Affiliations
Corresponding author
Electornic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table S1
List of smoke responsive genes (XLS 518 KB)
Supplementary Table S2
Cis-acting elements found in the predicted promoter sequence of smoke responsive genes (XLS 110 KB)
Supplementary Table S3
Frequency and significance of the GO terms appearing in the smoke responsive genes (XLS 102 KB)
Rights and permissions
About this article
Cite this article
Soós, V., Sebestyén, E., Juhász, A. et al. Stress-related genes define essential steps in the response of maize seedlings to smoke-water. Funct Integr Genomics 9, 231–242 (2009). https://doi.org/10.1007/s10142-008-0105-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-008-0105-8