Abstract
Proline accumulation and catabolism play significant roles in adaptation to a variety of plant stresses including osmotic stress, drought, temperature, freezing, UV irradiation, heavy metals and pathogen infection. In this study, the gene Δ1 -pyrroline-5-carboxylate dehydrogenase (P5CDH), which catalyzes the second step in the conversion of proline to glutamate, is characterized in a number of cereal species. P5CDH genes from hexaploid wheat, Triticum turgidum (durum wheat), Aegilops tauschii, Triticum monococcum, barley, maize and rice were shown to be conserved in terms of gene structure and sequence, present as a single copy per haploid, non-polyploid genome and located in evolutionarily conserved linkage groups. A wheat cDNA sequence was shown by yeast complementation to encode a functional P5CDH activity. A divergently-transcribed rab7 gene was identified immediately 5′ of P5CDH in all grasses examined, except rice. The rab7/P5CDH intergenic region in these species, which presumably encompasses 5′ regulatory elements of both genes, showed a distinct pattern of sequence evolution with sequences in juxtaposition to each ORF conserved between barley, wheat, A. tauschii and T. monococcum. More distal 5′ sequence in this intergenic region showed a higher rate of divergence, with no homology observed between these regions in the wheat and barley genomes. Maize and rice showed no similarity in regions 5′ of P5CDH when compared with wheat, barley, and each other, apart from a 22 bp region of conserved non-coding sequence (CNS) that is similar to a proline response element identified in the promoter of the Arabidopsis proline dehydrogenase gene. A palindromic motif similar to this cereal CNS was also identified 5′ of the Arabidopsis AtP5CDH gene showing conservation of this sequence in monocot and dicot lineages.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn S, Tanksley SD (1993) Comparative linkage maps of the rice and maize genomes. Proc Natl Acad Sci USA 90:7980–7984
Ahn S, Anderson JA, Sorrells ME, Tanksley SD (1993) Homeologous relationships of rice, wheat and maize chromosomes. Mol Gen Genet 241:483–490
Ayliffe MA, Frost DV, Finnegan EJ, Lawrence GJ, Anderson PA, Ellis JG (1999) Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant J 17(3):287–292
Ayliffe MA, Roberts JK, Mitchell HJ, Zhang R, Lawrence JG, Ellis JG, Pryor AJ (2002) A plant gene upregulated at rust infections sites. Plant Physiol 129:169–180
Chalmers KJ, Campell AW, Kretschmer J, Karakousis A, Henschke PH, Pierens S, Harker N, Pallotta M, Cornish GB, Shariflou MR, Rampling LR, McLauchlan A, Dagard G, Sharp PJ, Holton TA, Sutherland MW, Appels R, Langridge P (2001) Construction of three linkage maps in bread wheat, Triticum aestivum. Aust J Agric Res 52:1089–1119
Davis GL, McMullen MD, Baysdorfer C, Musket T, Grant D, Staebell M, Xu G, Polacco M, Koster L, Melia-Hancock S, Houchins K, Chao S, Coe EH (1999) A maize map with sequenced core markers, grass genome reference points and 932 expressed sequence tagged sites (ESTs) in a 1736-locus map. Genetics 152:1137–1172
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223
Delauney AJ, Hu C-AA, Kavi Kishor PB, Verma DPS (1993) Cloning of orthinine-δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268:18673–18678
Deuschle K, Funck D, Hellman H, Daeschner K, Binder S, Frommer WB (2001) A nuclear gene encoding mitochondrial Δ1 -pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. Plant J 27:345–355
Deuschle K, Funck D, Forlani G, Stansky H, Biehl A, Leister D, van der Graff E, Kunze R, Frommer WB (2004) The role of delta-1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16:3413–3425
Dvorak J, McGuire PE, Cassidy B (1988) Apparent sources of the A genomes of wheats inferred from polymorphism in abundance and restriction fragment length of repeated nucleotide sequences. Genome 30:680–689
Elthon TE, Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67:780–784
Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974
Guo H, Moose SP (2003) Conserved noncoding sequences among cultivated cereal genomes identify candidate regulatory sequence elements and patterns of promoter evolution. Plant Cell 15:1143–1158
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102
Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant towards exogenous proline application. Plant Physiol 123:779–790
Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of delta-1-pyrrilone-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122: 1129–1136
Hughes DW, Galua G (1988) Preparation of RNA from cotton leaves and pollen. Plant Mol Biol Report 6:253–257
Kaplinsky NJ, Braun DM, Penterman J, Goff SA, Freeling M (2002) Utility and distribution of conserved noncoding sequences in the grasses. Proc Natl Acad Sci USA 99:6147–6151
Kimber G, Sears ER (1987) Evolution of the genus Triticum and the origin of cultivated wheat. In: Heyne EG (ed) Wheat and wheat improvement American Society of Agronomy, Madison, pp 154–164
Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of (delta)-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394
Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline, but downregulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I (2000) VISTA: Visualising global DNA sequence alignments of arbitrary length. Bioinformatics 16:1046–1047
Minet M, Dufour ME, Lacroute F (1992) Complementation of Saccharomyces cerevisae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J 2:417–422
Mitchell HJ, Ayliffe MA, Rashid K, Pryor AJ (2005) A rust inducible gene from flax (fis1) is involved in proline catabolism. Planta (in press)
Nanjo T, Kobayashi M, Yoshiba Y, Sanada Y, Wada K, Tsukaya H, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Biological functions of proline morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J 18:185–193
Nuoffer C, Balch WE (1994) GTPases: multifunctional molecular switches regulating vesicular traffic. Annu Rev Biochem 63: 949–990
Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K, Iida K, Maruyama K, Satoh S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring the expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. Plant J 34:868–887
Ramakrishna W, Dubcovsky J, Park Y-J, Busso C, Emberton J, SanMiguel P, Bennetzen (2002) Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 162:1389–1400
Roberts J, Pryor AJ (1995) Isolation of a flax (Linum usitatissimum) gene induced during susceptible infection by flax rust (Melampsora lini). Plant J 8:1–8
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard R (1984) Ribosomal DNA spacer-length polymorphism in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc Natl Acad Sci USA 81:8014–8018
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A laboratory manual, 2nd edn. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY
SanMiguel PJ, Ramakrishna W, Bennetzen JL, Busso CS, Dubcovsky J (2002) Transposable elements, genes and recombination in a 215 kb contig from wheat chromosome 5AM. Func Integr Genomics 2:70–80
Satoh R, Nakashima K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2002) ACTCAT, a novel cis-acting element for proline and hypoosmolarity responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis. Plant Physiology 130:709–719
Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103:771–781
Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Lui Z-D, Dubcovsky J, Keller B (2003) Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and AM genomes of wheat. Plant Cell 15:1186–1197
Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205
Acknowledgements
We wish to thank Luch Hac, Craig Jackson and Kim Newell for technical assistance and Professor M. Brandriss (Newark, NJ, USA) for providing yeast strain MB1472. This work was financially supported in part by Bayer and has been carried out in compliance with current laws governing genetic experimentation in Australia.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.-A. Grandbastien
Rights and permissions
About this article
Cite this article
Ayliffe, M.A., Mitchell, H.J., Deuschle, K. et al. Comparative analysis in cereals of a key proline catabolism gene.. Mol Genet Genomics 274, 494–505 (2005). https://doi.org/10.1007/s00438-005-0048-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-005-0048-x