Abstract
Two-dimensional gel electrophoresis of pea root and root hair proteins revealed the existence of at least 10 proteins present at elevated levels in root hairs. One of these, named RH2, was isolated and a partial amino acid sequence was determined from two tryptic peptides. Using this sequence information oligonucleotides were designed to isolate by PCR an RH2 cDNA clone. In situ hybridization studies with this cDNA clone showed that rh2 is not only expressed in root hairs, but also in root epidermal cells lacking these tubular outgrowths. During post-embryonic development the gene is switched on after the transition of protoderm into epidermis and since rh2 is already expressed in a globular pea embryo in the protoderm at the side attached to the suspensor, we conclude that the expression of rh2 is developmentally regulated. At the amino acid level RH2 is 95% homologous to the pea PR protein I49a. These gene encoding I49a is induced in pea pods upon inoculation with the pathogen Fusarium solani [12]. We postulate that rh2 contributes to a constitutive defence barrier in the root epidermis. A similar role has been proposed for chalcone synthase (CHS) and chitinase, pathogenesis-related protein that are also constitutively present in certain epidermal tissues.
Similar content being viewed by others
References
Bhuvaneswari TV, Bhagwat AA, Bauer WD: Transient susceptibility of root cells of four common legumes to nodulation by rhizobia. Plant Physiol 68: 1144–1149 (1981).
Bisseling T, van den Bos RC, van Kammen A: The effect of ammonium nitrate on the synthesis of nitrogenase and the concentration of leghaemoglobin in pea root nodules induced by Rhizobium leguminosarum. Biochim Biophys Acta 539: 1–11 (1978).
Caetano-Anolles G, Gresshoff PM: Alfalfa controls nodulation during the onset of Rhizobium-induced cortical cell division. Plant Physiol 95: 366–373 (1991).
Chiang CC, Hadwiger LA: Cloning and characterization of a disease resistance response gene in pea inducible by Fusarium solani. Mol Plant-Microbe Interact 3: 78–85 (1990).
Clowes FAL: Apical Meristems. Blackwell, Oxford (1961).
Cox KH, Goldberg RB: Analysis of plant gene expression. In: Shaw CH (ed) Plant Molecular Biology: A Practical Approach. IRL Press, Oxford (1988).
de Vries SC, Springer J, Wessels JHG: Diversity of abundant mRNA sequences and patterns of protein synthesis in etiolated and screened pea seedlings. Planta 156: 129–135 (1982).
Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B: Cellular organisation of the Arabidopsis thaliana root. Development 119: 71–84 (1993).
Esau K: Anatomy of Seed Plants. John Wiley, New York (1977).
Fisher RF, Long SR: Rhizobium-plant signal exchange. Nature 357: 655–660 (1992).
Franssen HJ, Vijn I, Yang W, Bisseling T: Developmental aspects of the Rhizobium-legume interaction. Plant Mol Biol 19: 89–107 (1992).
Fristensky B, Riggleman RC, Wagoner W, Hadwiger LA: Gene expression in susceptible and disease resistant interactions of peas induced with Fusarium solani pathogens and chitosan. Physiol Plant Path 27: 15–28 (1985).
Gerhold DL, Dazzo FB, Gresshoff PM: Selective removal of seedling root hairs for studies of the Rhizobium-legume interaction. J Microbiol Meth 4: 95–102 (1985).
Gloudemans T, Bhuvaneswari TV, Moerman M, van Brussel T, van Kammen A, Bisseling T: Involvement of Rhizobium leguminosarum nodulation genes on gene expression in pea root hairs. Plant Mol Biol 12: 157–167 (1989).
Gloudemans T, Moerman M, van Beckum J, Gundersen J, van Kammen A, Bisseling T: Identification of plant genes involved in the Rhizobium leguminosarum-pea root hair interaction. In: Bothe H, de Bruyn FJ, newton WE (eds) Nitrogen Fixation: A Hundred Years After, pp. 611–616. Gustav Fischer Verlag, Stuttgart (1988).
Govers F, Gloudemans T, Moerman M, van Kammen A, Bisseling T: Expression of plant genes during the development of pea root nodules. EMBO J 4: 861–867 (1985).
Hahlbrock K, Scheel D: Physiology and molecular biology of phenyl propanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40: 347–369 (1989).
Horvath B, Heidstra R, Lados M, Moerrman M, Spaink HP, Promé JC, van Kammen A, Bisseling T: Lipooligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J 4: 727–733 (1993).
Krause A, Broughton WJ: Proteins associated with root-hair deformation and nodule initiation in Vigna unguiculata. Mol Plant-Microbe Interact 5: 96–103 (1992).
Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé K, Dénarié J: Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acetylated glucosamine oligosaccharide signal. Nature 344: 781–784 (1990).
Lindsey K, Toppey JF: Embryogenesis: a question of pattern. J Exp Bot 44: 359–374 (1993).
Marinos NG: Embryogenesis of the pea (Pisum sativum). I. The cytological environment of the developing embryo. Protoplasma 70: 261–279 (1970).
Matton DP, Brisson N: Cloning, expression and sequence conservation of pathogenesis-related gene transcripts of potato. Mol Plant-Microbe Interact 6: 325–331 (1989).
Morrissey JH: Silver stain of proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem 117: 307–310 (1981).
Reeve RM: Late embryogeny and histogenesis in Pisum. Am J Bot 35: 591–602 (1948).
Röhm M, Werner D: Isolation of root hairs from seedlings of Pisum sativum. Identification of root hair specific proteins by in situ labeling. Physiol Plant 69: 129–136 (1987).
Samac DA, Shah DM: Developmental and pathogen-induced activation of the Arabidopsis acidic chitanase promotor. Plant Cell 3: 1063–1072 (1991).
Sambrook J, Fritsch FF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Press, Cold Spring Harbor, NY (1989).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with cain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Schiefelbein JW, Benfey PN: The development of plant roots: new approaches to underground problems. Plant Cell 3: 1147–1154 (1991).
Schiefelbein JW, Sommerville C: Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2: 235–243 (1990).
Schmid J, Doerner PW, Clouse SD, Dixon RA, Lamb CJ: Developmental and environmental regulation of a bean chalcone synthase promotor in transgenic tobacco. Plant Cell 2: 619–631 (1990).
Spaink HJ, Sheeley DM, van Brussel AAN, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJJ: A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125–130 (1991).
van der Straeten D, Van Wiemeersch, Van Damme J, Goodman H, Van Montagu M: In: Clijsters H, Van Poucke M (eds) Biochemical and Physiological Aspects of Ethylene production in Lower and Higher Plants, pp. 93–100 (1989).
van de Wiel C, Scheres B, Franssen HJ, van Lierop MJ, van Lammeren A, van Kammen A, Bisseling T: The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J 9: 1–7 (1990).
Vijn I, Das Neves L, van Kammen A, Franssen H, Bisseling T: Nod factors and nodulation in plants. Science 260: 1764–1765 (1993).
Walter MH, Liu JW, Grand C, Lamb CJ, Hess D: Bean pathogenesis-related (PR) proteins deduced from elicitor-induced transcripts are members of a ubiquitous new class of conserved PR proteins including pollen allergens. Mol Gen Genet 222: 353–360 (1990).
Weier TE, Stocking CR, Barbour MG, Rost TL: Botany: An Introduction to Plant Biology. Wiley and sons, New York (1982).
Yang WC, Cantor Creemers HCJ, Hogendijk P, Katinakis P, Wijffelman CA, Franssen HJ, van Kammen A, Bisseling T: In situ localization of chalcone synthase mRNA in pea root nodule development. Plant J 2: 143–151 (1992).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mylona, P., Moerman, M., Yang, WC. et al. The root epidermis-specific pea gene RH2 is homologous to a pathogenesis-related gene. Plant Mol Biol 26, 39–50 (1994). https://doi.org/10.1007/BF00039518
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00039518