I am generally interested in the ecology and evolution of plant-enemy interactions, and have studied a number of systems over the course of my career. At the moment, we are focusing quite strongly on the coevolutionary interactions between Arabidopsis thaliana and its bacterial pathogens. This work was originally motivated by a desire to ask whether there is a signature of coevolutionary arms evident in the resistance genes of A. thaliana. We have found, contrary to expectation, that R genes retain allelic variation in resistance for millions of years. That is, they show evidence of ancient balanced polymorphisms. This has led us to investigate how selection acts to maintain genetic variation, both by performing field and greenhouse experiments and by collaborating on models of the coevolutionary process. In addition, we have been working to understand the evolution of virulence in natural bacterial pathogens of A. thaliana. A common approach to all this work is to use genetic engineering to understand the ecological importance of particular genes, and to link short-term ecological and micro-evolutionary processes with the long-term evolutionary patterns that they generate. Our ultimate goal is to understand how reciprocal selection shapes the interactions between plants and their pathogens.
(1) The evolution of resistance in A. thaliana
Until recently, there was general belief that gene-for-gene interactions between plants and their pathogens undergo coevolutionary arms races. By this, we mean that resistance specificities on the part of the plant undergo a dynamical turnover in response to a change in avirulence alleles in the pathogen, and vice-versa. Acceptance of an arms race model had been fostered by the observation in agriculture that pathogens can rapidly overcome novel resistance traits that are bred into crops. This illustrates that pathogens can be evolutionarily dynamic, as is anticipated under an arms race. We have employed a molecular evolutionary approach to seek signatures of arms race dynamics in A. thaliana R genes. Surprisingly, instead of exhibiting arms race dynamics, we found evidence of balancing selection at Rpm1, the first R gene that we studied.
Having found evidence for balancing selection at Rpm1, we sought to test whether this locus was somehow anomalous or revealed an evolutionary history that was common to other R-genes. Surprisingly, we repeated the general observation of ancient balanced polymorphisms at two additional R-genes (Rps5 and Rps2) that also have simple genetic architectures. In addition, we examined a complex locus, Rpp8, which also shows a surprising pattern; variation is extensive, with essentially every individual carrying a distinct allele, yet allelic variation is old. Thus, rather than suggesting a dynamical turnover of alleles, it appears that, for this set of loci, balancing selection has acted to maintain alternative alleles for millions of years.
(2) Selective forces promoting the maintenance of resistance and susceptibility alleles
How does selection promote the long-term maintenance of alternative alleles? For this work, we have focused on the R- gene Rpm1, which exists as an insertion-deletion polymorphism in A. thaliana. Since A. thaliana is a highly selfing species, we have excluded overdominance as a likely explanation and instead have tested for a cost of resistance. Our previous work, and the work of others, has revealed that costs can be detected for several resistance traits. However, R-genes are not expected to reveal detectable costs because they are recognition proteins expressed at very low levels. To test for costs of resistance, we used genetic engineering to create transgenic isolines that would allow such a comparison, and were surprised to find large costs associated with Rpm1 presence. This result raises many questions about the generality of costs of R-gene resistance, the physiological mechanism underlying the cost, and the relationship between evolutionary history and costs of resistance, that we are pursuing.
A related observation that we have made is that resistant plants that are infected can fare less well than susceptible isolines that are infected, at least in some environments. This is a surprising observation in that resistance is typically believed to be beneficial when plants are under attack. Two things contribute to this outcome. First, A. thaliana has a tremendous ability to tolerate disease. Indeed, infected individuals have a characteristic regrowth response and susceptible individuals respond more strongly than resistant individuals. This is reminiscent of the well-characterized regrowth response that we previously studied in scarlet gilia. Second, the resistance response itself is rather costly and places a metabolic drain on resistant individuals. We have produced a model that suggests that costs in the presence of disease may contribute to the maintenance of polymorphisms, although the relevance of these results in a natural field setting remains to be tested.
(3) The ecology and evolution of the bacterial pathogens of A. thaliana
A. thaliana is attacked by several bacterial pathogens, the most prevalent of these is Pseudomonas viridiflava, which is a soft rot pathogen. Up to 40% of A. thaliana plants can be infected with P. viridiflava within Midwestern populations; the rate of infection is variable and positively correlated with A. thaliana density. We study of several genomic fragments in a sample of 96 P. viridiflava strains reveals two distinct groups of isolates. There is unambiguous evidence for recombination among isolates within, but not between, groups, suggesting the presence of cryptic species.
The virulence of these (and other) pathogens is encoded, in large part, by pathogencity islands. We have discovered that P. viridiflava harbors two alternative pathogenicity islands, and that the presence or absence of each exists as an ancient balanced polymorphism. These alternative pathogenicity islands differ in their virulence, but there is still much to learn about the ecological and evolutionary forces that explain this unusual polymorphism. We are excited to begin such studies. In addition, we have begun exploring the molecular evolution of avirulence genes (genes that are recognized by plant R genes) in this pathogen, and see clear signatures of selection.
(4) Genome scale patterns of linkage disequilibrium and polymorphism in A. thaliana
As part of a 2010 project in collaboration with Magnus Nordborg (USC), we are creating a haplotype map of A. thaliana by assaying polymrophism in ~ 1500 500-bp fragments distributed throughout the genome of 96 A. thaliana accessions. These data also allow detailed characterization of patterns of polymorphism within the genome, as well as investigation of the demographic history and population structure of this species. Such work is ongoing. We hope to extend this project to develop A. thaliana as a species in which linkage disequilibrium will be possible. For more information, see walnut.usc.edu/2010.html.
In related work, we are completing a more comprehensive examination of R-gene evolution in these same 96 A. thaliana accessions. To date, we have sequenced about 27 LRR regions. Although the data await analysis, it is clear that ancient balanced polymorphisms characterize only one of several classes of Arabidopsis R-genes. A main goal for the immediate future is to fully characterize the evolutionary history of the family of R-genes, and in the longer term to understand the factors the lead to these alternative histories.
Representative Publications
Bergelson, J and MJ Crawley. 1992. Herbivory and
Ipomopsis aggregata: the disadvantages of being eaten. The American
Naturalist
139: 870-882.
Bergelson, J. 1994. The effects of genotype and
the environment on the costs of
resistance in lettuce. The American Naturalist 143:349-359.
Bergelson, J
and CB Purrington. 1996. Surveying patterns in the cost of
resistance in plants. The
American Naturalist 148: 536-558.
Bergelson, J, Purrington, CB, Palm, CJ and JC
L—pez-GutiŽrrez. 1996. Costs of
resistance: a test using transgenic Arabidopsis thaliana. Proceedings of the Royal
Society B
263: 1659-1663.
Purrington, CB and J Bergelson. 1997. Fitness
consequences of genetically engineered herbicide and antibiotic resistance in Arabidopsis
thaliana.
Genetics 145:
807-814.
Bergelson, J, Stahl, E, Dudek, S and M Kreitman. 1998. Genetic variation
within and among populations. Genetics 148: 1311-1323.
Bergelson, J, Purrington, CB and G
Wichmann. 1998. Male promiscuity
is increased in transgenic plants.
Nature
395:25.
Juenger, T and J Bergelson. 1998. Pairwise and
diffuse selection and the multiple herbivores of scarlet gilia, Ipomopsis
aggregata (Polemoniaceae). Evolution 52:1583-1592.
Stahl,
E, Dwyer, G, Mauricio, R, Kreitman, M and J Bergelson. 1999. Dynamics of
disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667-671.
Juenger,
T and J Bergelson. 2000. The
evolution of compensation to herbivory in scarlet gilia, Ipomopsis
aggregata;
herbivore-imposed selection and the quantitative genetics of tolerance traits. Evolution 54(3) 764-777.
Shonle,
I and J Bergelson. 2000.
Evolutionary ecology of the tropane alkaloids of Datura Stramonium L. (Solanaceae). Evolution 54(3) 778-788.
Cipollini,
D and J Bergelson. 2001. Plant
density and nutrient availability constrain the constitutive and wound-induced
expression of trypsin inhibitors in Brassica napus. Journal of Chemical Ecology 27:593-610.
Bergelson,
J, Kreitman, M, Stahl, EA and D Tian.
2001. Evolutionary dynamics
of R-genes
in plants. Science 292: 2281-2285.
Bergelson,
J., Dwyer, G and JJ Emerson.
2001. Models and data on
plant enemy coevolution. Annual
Review of Genetic 35:
469-99.
Nordborg,
M., Borevitz, JO, Bergelson, J, Berry, J, Chory, J, Hagenblad, J, Kreitman, K,
Maloof, JN, Noyes, T, Oefner, PJ, Stahl, E and D Weigel. 2002. The extent of linkage
disequilibrium in the highly selfing species, Arabidopsis thaliana. Nature Genetics 30(2): 190-3.
Tian,
D., Araki, H., Stahl, EA, Bergelson, J and M Kreitman. 2002. Signature of balancing selection in Arabidopsis. Proceedings of the National Academy
of Science USA.
99: 11525-530.
Jakob,
K., Goss, EM, Araki, H, Van, T, Kreitman, M and J Bergelson.
2002. Pseudomonas
viridiflava
and P. syringae
Đ natural pathogens of Arabidopsis thaliana. Molecular Plant
Microbe Interactions
15: 1195-1203.
Cipollini, DF, Purrington, CB and J Bergelson. 2003.
Costs of induced resistance. Special Feature on Induced Responses of Plants
towards Herbivory. . Basic and
Applied Ecology 4:79-89.
Mauricio,
R, Korves, T, Stahl, EA, Kreitman, M and J Bergelson. 2003. Natural selection for polymorphism in the disease
resistance gene Rps2 of Arabidopsis.
Genetics 163:735-746.
Tian,
D, Traw, MB, Chen J, Kreitman, M and J Bergelson. 2003. Pleiotropic fitness cost of Rpm1 resistance in Arabidopsis
thaliana. Nature 423: 74-77.
Traw,
MB, Kim, J, Enright, S, Cipollini, DF and J Bergelson. 2003. Negative
cross-talk between the salicylate and jasmonate-mediated pathways in the
Wassilewskija ecotype of Arabidopsis thaliana. Molecular Ecology 12, 1125-1135.
Korves,
T and J Bergelson. 2003. A
developmental response to pathogen infection in Arabidopsis thaliana. Plant Physiology 133: 339-347.
Traw,
MB and J Bergelson. 2003.
Interactive effects of jasmonic acid, salicylic acid, and gibberellin on the
induction of trichomes in Arabidopsis thaliana. Plant Physiology 133: 1367-1375.
Wichmann,
G. and J. Bergelson. 2004. avr
genes of Xanthamonas axonopodis pv. vesicatoria promote transmission
and enhance other fitness traits. Genetics, in press.
Korves,
T. and J. Bergelson. 2004. A novel fitness cost of R-gene resistance in the
presence of disease. The
American Naturalist,
in press.
Cipollini,
D., Enright, S, Traw, MB and J Bergelson. 2004. Salicylic acid inhibits
jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Molecular Ecology, in press.