Pamela Ronald on New Discoveries in Rice Research

New Hot Paper Commentary, March 2011

Pamela Ronald

Article: A Type I-Secreted, Sulfated Peptide Triggers XA21-Mediated Innate Immunity


Authors: Lee, SW;Han, SW;Sririyanum, M;Park, CJ;Seo, YS;Ronald, PC
Journal: SCIENCE, Volume: 326, Issue: 5954, Page: 850-853, Year: NOV 6 2009
Addresses: * Univ Calif Davis, Dept Plant Pathol, Davis, CA 95616 USA.
* Univ Calif Davis, Dept Plant Pathol, Davis, CA 95616 USA.

Photo credit: Roy Kaltschmidt, Lawrence Berkeley National Laboratory.

Pamela Ronald talks with ScienceWatch.com and answers a few questions about this month's New Hot Paper in the field of Plant & Animal Science.


SW: Why do you think your paper is highly cited?

In 1995 we showed that the rice XA21 resistance gene, encoding a protein with predicted leucine rich repeat (LRR), transmembrane, juxtamembrane, and intracellular kinase domains, conferred immunity to diverse strains of the Gram-negative bacterium, Xanthomonas oryzae pv. oryzae (Xoo; Song et al., 1995).

Subsequent discoveries in flies (Toll; Lemaitre et al., 1996), humans (Toll-like receptors; Medzhitov et al., 1997), mice (TLR4; Poltorak et al., 1998), and Arabidopsis (FLS2;L. Gomez-Gomez, T. Boller, Mol. Cell 5: 1003, 2000) revealed that animals and other plant species also carry membrane-anchored receptors with striking structural similarities to XA21 and that these receptors are also involved in microbial recognition and defense. Like XA21, these receptors typically associate with or carry non-RD (arginine-aspartic acid) kinases to control early events of innate immunity signaling (Dardick and Ronald, 2006).

Pam and Village Women in Bangladesh. Photo credit Gene Hettel, IRRI.
Pam and Village Women in Bangladesh. Photo credit Gene Hettel, IRRI.

View additional images at The RonalD Labratory Website (See also).

The predicted structure of XA21 immediately suggested a mechanism of action in which the extracellular domain would engage a microbial elicitor leading to signal transduction by the cytoplasmic domain. However, the structure of XA21 gave no clue as to the nature of the microbially derived molecule. The research presented in this paper demonstrates that XA21 binds to a highly conserved Type I secreted peptide, called AxYS22, and that sulfation is critical for recognition.

SW: Does it describe a new discovery, methodology, or synthesis of knowledge?

Yes this is a new discovery. Type 1 secreted peptides are abundant in the host environment but have not previously been shown to interact with host receptors. Thus this work presents new insights into host-microbe interactions. The research also demonstrate that sulfation of peptides likely occurs in bacteria, which has not yet been demonstrated. This work contributes to a growing body of research showing that sulfation mediates interaction between receptors and their ligands.

SW: Would you summarize the significance of your paper in layman's terms?

The mechanisms of plant and animal defense against microbes have historically been presumed to be separate and distinct. Beginning around the 1870s, studies of animal responses to infection revealed the existence of both "natural" or innate immunity, which involved the cells and molecules mediating host inflammatory responses, and adaptive immunity, which permitted the generation of cellular receptors with immense diversity and exquisite specificity for foreign macromolecules of almost any kind.

Lacking phagocytes, lymphocytes, antibodies, and many other parts of the animal armamentarium, it seemed that the plant response to disease must utilize a fundamentally different strategy. However, discoveries over the past 15 years demonstrate that the mechanisms that allow plants and animals to resist infection show impressive structural and strategic similarity. Remarkably, the elucidation of these mechanisms followed a common approach involving a concerted attack on the same basic questions. This paper answers a basic question: what molecules are recognized by the host as signatures of infection?

SW: How did you become involved in this research, and how would you describe the particular challenges, setbacks, and successes that you've encountered along the way?

"Rice feeds half the words people and is a model for other important staple food crops."

For a long time, the plant biology community believed that classically defined resistance genes, such as XA21, and receptors for microbial signatures, such as FLS2, governed distinctly different processes. With the demonstration that XA21 binds a highly conserved Xoo-derived peptide and the discovery that a mutation in FLS2 rendered Arabidopsis susceptible to the bacterial pathogen Pseudomonas syringae, these views have begun to change.

Our results now demonstrate that the definitions of pathogen-associated molecular patterns (PAMPs) and avr genes and those of disease-resistance genes and pattern recognition receptors (PRRs) cannot be strictly separated. In plants, a disease-resistance gene is merely the current single polymorphic point in the host genotype that confers resistance in a particular interaction. These can encode diverse proteins (although, to date, the great majority encodes intracellular nucleotide binding-LRR proteins). Hence, the term "R gene" is merely operational and mechanistically agnostic.

Likewise, the term "avirulence gene" remains useful as a broad term that indicates a gene that encodes any determinant of the specificity of the interaction with the host. Thus, this term can encompass some PAMPs and pathogen effectors (e.g., bacterial type III effectors and oomycete effectors) as well as any genes that control variation in the activity of those molecules.

SW: Do you foresee any social or political implications for your research?

Rice feeds half the words people and is a model for other important staple food crops. Thus basic discoveries in rice and application of this research to plant breeding and genetic engineering will lead to the development of new crop varieties that are resistance to disease. Such approaches will increase yield and reduce the need for pesticides. Because XA21 is also present in a human bacterial pathogen, new targets for drug treatments can be identified. Thus the results are relevant to human health and well-being.End

Pamela C. Ronald
Professor, Plant Pathology
University of California, Davis
Davis, CA, USA
and
Vice President of Feedstocks
Joint Bioenergy Institute
Emeryville, CA, USA

KEYWORDS: RICE Xa21 GENE, XANTHOMONAS ORYZAE PV ORYZAE, SULFATED SYNTHETIC PEPTIDE, DISEASE RESISTANCE, GENE, RICE, ARABIDOPSIS, FLAGELLIN, PLANTS, PERCEPTION, CAMPESTRIS, ACYLATION, ELICITOR.

 
 

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