The plant basal immune system can detect broadly present microbe-associated molecular patterns (MAMPs, also called PAMPs) and induce defenses, but adapted microbes express a suite of effector proteins that often act to suppress these defenses. Plants have evolved other receptors (R proteins) that detect these pathogen effectors and activate strong defenses. Pathogens can subsequently alter or delete their recognized effectors to avoid defense elicitation, at risk of a fitness cost associated with loss of those effectors. Significant research progress is revealing, among other things, mechanisms of MAMP perception, the host defense processes and specific host proteins that pathogen effectors target, the mechanisms of R protein activation, and the ways in which pathogen effector suites and R genes evolve. These findings carry practical ramifications for resistance durability and for future resistance engineering. The present review uses numerous questions to help clarify what we know and to identify areas that are ripe for further investigation.

Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions

The latest previous comprehensive review of allelopathy (Rice, 1974) covered research done primarily prior to 1973. There have been numerous reviews published in recent years on specific phases of allelopathy (see III), but most of them covered research results published primarily through 1972 also. This review has been restricted, therefore, largely to research conducted subsequent to 1972, except for background information and significant papers overlooked in previous reviews. There has been almost an exponential increase in the rate of publication of papers concerned with allelopathy. Research has been particularly active in relation to the roles of allelopathy in agriculture, forestry, phytopathology, patterning of vegetation, algal succession, and old-field succession. Our increasing knowledge of the conditions under which certain crop residues cause allelopathic effects to subsequent crops should enable us soon to guard against such effects. We are on the threshold of breeding crop plants that will inhibit the chief weeds in a given area through allelopathic action, and thus decrease the need for synthetic weed killers. Our understanding of allelopathic interactions of various plant species has already been used advantageously in reforestation, and future developments are very encouraging. Our increasing knowledge of allelopathy is aiding greatly in our understanding of many ecological phenomena, such as succession and patterning of vegetation. Evidence is mounting that inhibition of nitrification increases as succession progresses toward the climax vegetation, at least in many vegetation types. This leads to a decrease in the loss of nitrogen. Addition of inhibitors to arable lands to prevent nitrification has proved to be valuable in preventing loss of nitrogen and in increasing crop yields. There has been a rapid advance in our knowledge of mechanisms of action of known allelopathic compounds, at increasingly more fundamental levels. We have known for several years, for example, that some of these compounds inhibit uptake of various minerals, but have not known the mechanism of the action. Recent research indicates this may be due, at least in part, to inhibition of a plasma membrane ATPase that is involved with ion absorption. A thorough knowledge of mechanisms of action of allelochemics is essential to our overall understanding and appreciation of the field of allelopathy.

Allelopathy—An update

Phytoalexins: enzymology and molecular biology.

Activation of plant defense genes was investigated by analysis of transcripts completed in vitro by isolated nuclei. Elicitor treatment of suspension-cultured bean (Phaseolus vulgaris L.) cells caused marked transient stimulation of transcription of genes encoding apoproteins of cell wall hydroxyproline-rich glycoproteins (HRGP) and the phenylpropanoid biosynthetic enzymes phenylalanine ammonia-lyase (PAL) and chalcone synthase (CHS), concomitant with the onset of rapid accumulation of the respective mRNAs and hence expression of the phytoalexin (PAL, CHS), lignin (PAL), and HRGP defense responses. While there was a lag of 2 h prior to stimulation of HRGP gene transcription, induction of the transcription of PAL and CHS genes occurred within 5 min of elicitor treatment. Induction of transcription of PAL, CHS, and HRGP genes was also observed in wounded hypocotyls and in infected hypocotyls during race-cultivar-specific interactions with the fungus Colletotrichum lindemuthianum, the causal agent of anthracnose. Transcriptional activation occurred not only in directly infected tissue but also in distant, hitherto uninfected tissue, indicating intercellular transmission of an endogenous signal for defense gene activation. It is concluded that transcriptional activation of defense genes characteristically underlies induction of the corresponding defense responses and expression of disease resistance.

Transcriptional activation of plant defense genes by fungal elicitor, wounding, and infection.

Summary

1. Induced resistance of plants to incompatible races of their microbial pathogens is often characterized by rapid cell death (the hypersensitive response) and the accumulation of low-Mr antimicrobial compounds termed phytoalexins. There is much indirect evidence to support a major role for phytoalexin induction as an event determining host resistance, and genetical analysis of race-specific pathogen-host interactions predicts that induced resistance occurs via interaction between a pathogen avirulence gene product and a host resistance gene product. Elicitors (inducing agents) of phytoalexin accumulation are possible candidates for the active products directly or indirectly resulting from the expression of microbial avirulence genes. The present review considers the process of phytoalexin induction, at the molecular level, from the fungal elicitor to the early changes in host gene expression associated with its action.



2. A number of microbial polysaccharides, glycoproteins, pectic enzymes, peptides and fatty acids have potent elicitor activity.



3. The results of studies on the purification and characterization of microbial elicitors depend on the nature of the bioassay used. Methods for elicitor extraction may lead to artifacts or loss of race specificity.



4. Elicitors isolated from plant pathogens may be race-specific or race-non-specific. In cases where only race-non-specific elicitors can be shown, race-specific induction of phytoalexins may result from the action of enhancer or suppressor molecules. Fungal glucans have been proposed as candidates to act in both these roles.



5. Molecular genetic approaches to the identification of phytopathogenic bacterial avirulence genes may help to prove or disprove the role of elicitors of the phytoalexin response as agents responsible for the induction of host resistance. Similar analyses, involving genetic transformation, should soon be possible for phytopathogenic fungi.



6. Studies on the nature of host receptors for microbial elicitors are still in their infancy. Such receptors are probably localized in the plant plasma membrane, and elicitation results in often striking changes in host membrane properties.



7. Cyclic 3′,5′-adenosine monophosphate and polyamines do not appear to act in plants as intracellular transducers of the phytoalexin response. Interest is now being shown in a possible role for calcium in intracellular signalling.



8. Plant cells contain endogenous elicitor molecules whose synthesis or release may play a role in the intercellular transmission of the phytoalexin response. The main candidates for endogenous elicitors are pectic fragments of the host cell wall, although no direct evidence for their involvement in plant-pathogen interactions is available. Pectic fragments may act as synergists in parallel with, rather than as couplers in series with, microbial elicitors. The role of ethylene as a response coupler for induced resistance phenomena is difficult to assess.



9. Some elicitors may themselves move to the host cell nucleus, although whether this is their effective site of action remains unclear.



10. Induction of the phytoalexin response is associated with specific changes in host gene expression related to the selective induction of new mRNA species and enzyme activities.



11. Progress is now being made in the characterization of enzymes specific for phytoalexin biosynthesis. Enzyme induction and/or infection appears to involve rapid modulation of gene transcription, although some post-translational events may also be involved in determining induction patterns.



12. Work is now commencing on the sequencing of the genes encoding elicitor-inducible enzymes. Multigene families have been identified for phenylalanine ammonia-lyase and chalcone synthase.



13. Phytoalexin accumulation may be accompanied by the rapid induction of ethylene biosynthesis and the expression of genes encoding activities involved in the synthesis of hydroxyproline-rich glycoproteins.



14. Pectic endogenous elicitors of phytoalexin accumulation are also active as inducers of systemic proteinase inhibitor synthesis in some solanaceous species.



15. Results of studies on the mechanisms of signal transmission and differential gene expression in relation to active defence reactions should be of relevance to many other aspects of the plant's response to environmental stimuli at the physiological, biochemical and molecular genetical levels.

The phytoalexin response: elicitation, signalling and control of host gene expression

General plant resistance to pathogenic attack by a myriad of microorganisms, viruses, nematodes, and insects are reviewed. Specifically discussed are: The role of the cell wall and wall-degrading enzymes in infective processes; an hypothesis to account for varietal specificity in gene-for-gene host-pathogen systems; examples which demonstrate that cell surface recognition phenomena are mediated through the interaction of carbohydrate-containing macromolecules and proteins; elicitors of phytoalexin production; and further consideration of the hypothesis and how the gene-for-gene relationship may have evolved. (JWP)

Carbohydrates, Proteins, Cell Surfaces, and the Biochemistry of Pathogenesis

A polysaccharide from the fungal pathogen Colletotrichum lindemuthianum causes browning and phytoalexin production when applied to the cut surfaces of bean (Phaseolus vulgaris) cotyledons and hypocotyls. The application of an amount of polysaccharide equivalent to less than 100 ng of glucose will elicit this response in the bean tissues. The polysaccharide has been isolated both from culture filtrates and from the mycelial walls of the fungus. Purification of the polysaccharide involved anion and cation exchange chromatography and gel filtration. The polysaccharide has an apparent molecular weight between 1,000,000 and 5,000,000 daltons, and consists predominantly of 3- and 4-linked glucosyl residues.

Anne J. Anderson-Prouty

Papers

Carbohydrates, Proteins, Cell Surfaces, and the Biochemistry of Pathogenesis

Host-Pathogen Interactions: VIII. Isolation of a Pathogen-synthesized Fraction Rich in Glucan That Elicits a Defense Response in the Pathogen's Host.

Viii. isolation of a pathogen-synthesized fraction rich in glucan that elicits a defense response in the pathogen's host'