Abstract
Expression of the fis1 gene from flax (Linum usitatissimum) is induced by a compatible rust (Melampsora lini) infection. Infection of transgenic plants containing a beta-glucuronidase (GUS) reporter gene under the control of the fis1 promoter showed that induction is highly localized to those leaf mesophyll cells within and immediately surrounding rust infection sites. The level of induction reflects the extent of fungal growth. In a strong resistance reaction, such as the hypersensitive fleck mediated by the L6 resistance gene, there is very little fungal growth and a microscopic level of GUS expression. Partially resistant flax leaves show levels of GUS expression that were intermediate to the level observed in the fully susceptible infection. Sequence and deletion analysis using both transient Agrobacterium tumefaciens expression and stable transformation assays have shown that the rust-inducible fis1 promoter is contained within a 580-bp fragment. Homologs of fis1 were identified in expressed sequence tag databases of a range of plant species including dicots, monocots, and a gymnosperm. Homologous genes isolated from maize (Zea mays; mis1), barley (Hordeum vulgare; bis1), wheat (Triticum aestivum; wis1), and Arabidopsis encode proteins that are highly similar (76%-82%) to the FIS1 protein. The Arabidopsis homologue has been reported to encode a delta1-pyrroline-5-carboxylate dehydrogenase that is involved in the catabolism of proline to glutamate. RNA-blot analysis showed that mis1 in maize and the bis1 homolog in barley are both up-regulated by a compatible infection with the corresponding species-specific rust. The rust-induced genes homologous to fis1 are present in many plants. The promoters of these genes have potential roles for the engineering of synthetic rust resistance genes by targeting transgene expression to the sites of rust infection.
MeSH Terms
1-Pyrroline-5-Carboxylate Dehydrogenase
Amino Acid Sequence
Arabidopsis/genetics
Flax/genetics,microbiology
Fungi/growth & development
Gene Expression Regulation, Plant
Glucuronidase/genetics,metabolism
Hordeum/genetics
Molecular Sequence Data
Oxidoreductases Acting on CH-NH Group Donors/genetics,metabolism
Plant Diseases/genetics,microbiology
Plant Leaves/genetics,microbiology
Plant Proteins/genetics,metabolism
Plants, Genetically Modified
Proline/metabolism
Promoter Regions, Genetic/genetics
Recombinant Fusion Proteins/genetics,metabolism
Sequence Homology, Amino Acid
Triticum/genetics
Up-Regulation
Zea mays/genetics
Chemicals
Plant Proteins
Recombinant Fusion Proteins
Proline
FIS1 protein, Linum usitatissimum
1-Pyrroline-5-Carboxylate Dehydrogenase
Oxidoreductases Acting on CH-NH Group Donors
Glucuronidase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ayliffe Michael A
Commonwealth Scientific and Industrial Research Organization, Division of Plant Industry, Box 1600, Canberra, Australian Capital Territory 2601, Australia.
[email protected]
Roberts James K
Mitchell Heidi J
Zhang Ren
Lawrence Gregory J
Ellis Jeffrey G
Pryor Tony J
References (25)
25 references, click to expand
-
GTPases: multifunctional molecular switches regulating vesicular traffic.
Annu Rev Biochem. 1994;63:949-90
PMID: 7979258
-
Instability of the L6 gene for rust resistance in flax is correlated with the presence of a linked Ac element.
Plant J. 1993 Oct;4(4):659-69
PMID: 8252068
-
Developmental and tissue-specific expression of a tomato anionic peroxidase (tap1) gene by a minimal promoter, with wound and pathogen induction by an additional 5'-flanking region.
Plant Mol Biol. 1993 Jun;22(3):475-90
PMID: 8329686
-
Homologues of wheat ubiquitin-conjugating enzymes--TaUBC1 and TaUBC4 are encoded by small multigene families in Arabidopsis thaliana.
Plant Mol Biol. 1994 Feb;24(4):651-61
PMID: 8155884
-
Improved method for the isolation of RNA from plant tissues.
Anal Biochem. 1987 May 15;163(1):16-20
PMID: 2441623
-
Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library.
Mol Plant Microbe Interact. 1997 May;10(4):427-37
PMID: 9150592
-
Cutinase gene disruption in Fusarium solani f sp pisi decreases its virulence on pea.
Plant Cell. 1994 Jul;6(7):935-45
PMID: 8069105
-
Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application.
Plant Physiol. 2000 Jun;123(2):779-89
PMID: 10859207
-
Predicting subcellular localization of proteins based on their N-terminal amino acid sequence.
J Mol Biol. 2000 Jul 21;300(4):1005-16
PMID: 10891285
-
Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism.
Mol Plant Pathol. 2000 Mar 1;1(2):99-113
PMID: 20572957
-
A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae.
Mol Plant Microbe Interact. 1997 May;10(4):438-45
PMID: 9150593
-
Isolation of a flax (Linum usitatissimum) gene induced during susceptible infection by flax rust (Melampsora lini).
Plant J. 1995 Jul;8(1):1-8
PMID: 7655501
-
Root-knot nematode--directed expression of a plant root--specific gene.
Science. 1994 Jan 14;263(5144):221-3
PMID: 17839183
-
Differential gene expression in p53-mediated apoptosis-resistant vs. apoptosis-sensitive tumor cell lines.
Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13009-14
PMID: 11069295
-
Changes in two ribonuclease isozymes during rust infection of flax cotyledons.
Plant Physiol. 1982 Jan;69(1):205-9
PMID: 16662159
-
Cloning of a gene expressed during appressorium formation by Colletotrichum gloeosporioides and a marked decrease in virulence by disruption of this gene.
Plant Cell. 1995 Feb;7(2):183-93
PMID: 7756829
-
A comprehensive set of sequence analysis programs for the VAX.
Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95
PMID: 6546423
-
The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N.
Plant Cell. 1995 Aug;7(8):1195-206
PMID: 7549479
-
Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana.
Plant J. 1999 Apr;18(2):185-93
PMID: 10363370
-
Analysis of alternative transcripts of the flax L6 rust resistance gene.
Plant J. 1999 Feb;17(3):287-92
PMID: 10097386
-
Conversion of compatible plant-pathogen interactions into incompatible interactions by expression of the Pseudomonas syringae pv. syringae 61 hrmA gene in transgenic tobacco plants.
Plant J. 2000 Jul;23(2):205-13
PMID: 10929114
-
Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea.
Plant Cell. 1993 Nov;5(11):1575-90
PMID: 8312740
-
A nuclear gene encoding mitochondrial Delta-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity.
Plant J. 2001 Aug;27(4):345-56
PMID: 11532180
-
Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region.
Plant Cell. 1997 Apr;9(4):641-51
PMID: 9144966
-
Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics.
Proc Natl Acad Sci U S A. 1984 Dec;81(24):8014-8
PMID: 6096873