Spatial variation in disease resistance: from molecules to metapopulations.
Variation in disease resistance is a widespread phenomenon in wild plant-pathogen associations. Here, we review current literature on natural plant-pathogen associations to determine how diversity in disease resistance is distributed at different hierarchical levels - within host individuals, within host populations, among host populations at the metapopulation scale and at larger regional scales.We find diversity in resistance across all spatial scales examined. Furthermore, variability seems to be the best counter-defence of plants against their rapidly evolving pathogens. We find that higher diversity of resistance phenotypes also results in higher levels of resistance at the population level.Overall, we find that wild plant populations are more likely to be susceptible than resistant to their pathogens. However, the degree of resistance differs strikingly depending on the origin of the pathogen strains used in experimental inoculation studies. Plant populations are on average 16% more resistant to allopatric pathogen strains than they are to strains that occur within the same population (48 % vs. 32 % respectively).Pathogen dispersal mode affects levels of resistance in natural plant populations with lowest levels detected for hosts of airborne pathogens and highest for waterborne pathogens.Detailed analysis of two model systems, Linum marginale infected by Melampsora lini, and Plantago lanceolata infected by Podosphaera plantaginis, show that the amount of variation in disease resistance declines towards higher spatial scales as we move from individual hosts to metapopulations, but evaluation of multiple spatial scales is needed to fully capture the structure of disease resistance.Synthesis: Variation in disease resistance is ubiquitous in wild plant-pathogen associations. While the debate over whether the resistance structure of plant populations is determined by pathogen-imposed selection versus non-adaptive processes remains unresolved, we do report examples of pathogen-imposed selection on host resistance. Here we highlight the importance of measuring resistance across multiple spatial scales, and of using sympatric strains when looking for signs of coevolution in wild plant-pathogen interactions.
CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
Anna-Liisa
AL
Laine
Jeremy J
JJ
Burdon
Peter N
PN
Dodds
Peter H
PH
Thrall
Am Nat. 2008 May;171(5):658-68
18419564
Plant J. 1997 Oct;12(4):757-68
9375391
Nat Genet. 2002 Dec;32(4):569-77
12457190
New Phytol. 2006;171(1):137-44
16771989
Evolution. 2000 Aug;54(4):1102-15
11005280
Evolution. 2005 Jan;59(1):70-80
15792228
Nat Rev Genet. 2010 Aug;11(8):539-48
20585331
Evolution. 1994 Oct;48(5):1564-1575
28568407
Evolution. 2007 Aug;61(8):1812-22
17683425
J Evol Biol. 2008 Sep;21(5):1418-27
18557795
Evolution. 1999 Aug;53(4):1259-1267
28565537
Am Nat. 2009 Sep;174(3):308-20
19627233
Evolution. 1985 Jul;39(4):713-723
28561354
Curr Opin Plant Biol. 2002 Aug;5(4):339-44
12179968
Mol Ecol. 2008 Nov;17(22):4912-23
19140981
Science. 2003 Mar 14;299(5613):1680-1
12637729
Mol Biol Evol. 2009 Nov;26(11):2499-513
19633228
Evolution. 1994 Oct;48(5):1423-1437
28568406
Heredity (Edinb). 2003 Oct;91(4):345-52
14512948
Nat Rev Genet. 2007 May;8(5):382-93
17404584
Annu Rev Phytopathol. 2006;44:19-39
16343053
Oecologia. 1988 May;75(4):535-538
28312428
J Evol Biol. 2005 Jul;18(4):930-8
16033565
Evolution. 1991 Feb;45(1):205-217
28564067
J Evol Biol. 2007 Sep;20(5):1665-73
17714283
Genome Res. 1998 Nov;8(11):1113-30
9847076
Proc Biol Sci. 2006 Jun 22;273(1593):1501-6
16777744
Evolution. 1999 Apr;53(2):395-407
28565431
J Acquir Immune Defic Syndr. 2001 Jul 1;27(3):277-80
11464148
Evolution. 1999 Aug;53(4):1318-1324
28565518
Trends Genet. 2003 Dec;19(12):667-71
14642742
Nature. 2003 May 1;423(6935):74-7
12721627
Curr Opin Plant Biol. 2008 Apr;11(2):135-43
18329329
Plant Cell. 2006 Nov;18(11):2919-28
17114357
Proc Biol Sci. 2006 Apr 22;273(1589):1031-8
16627290
Nature. 2000 Aug 17;406(6797):718-22
10963595
J Evol Biol. 2010 Jan;23(1):87-97
19895655
Evolution. 1997 Oct;51(5):1416-1426
28568641
Science. 2009 May 8;324(5928):755-6
19423818
Evolution. 1988 Nov;42(6):1166-1171
28581071
Oecologia. 1996 Jan;105(2):205-213
28307084
Am Nat. 2000 Aug;156(2):156-174
10856199
New Phytol. 2004 Jun;162(3):729-743
33873775
Evolution. 2007 Feb;61(2):368-76
17348946
Proc Biol Sci. 2006 Feb 7;273(1584):267-73
16543168
Science. 2003 Mar 14;299(5613):1735-7
12637745
Genome Biol. 2003;4(9):227
12952527
Annu Rev Immunol. 1998;16:593-617
9597143
Theor Popul Biol. 1970 Aug;1(2):140-64
5527629
Evolution. 1991 Nov;45(7):1618-1627
28564135
Mol Plant Pathol. 2009 Jul;10(4):449-57
19523099
Mol Ecol. 2003 Jan;12(1):263-73
12492894
Evolution. 2007 Jan;61(1):27-41
17300425
Science. 2001 Jun 22;292(5525):2281-5
11423651
Annu Rev Phytopathol. 1996;34:29-50
15012533
Nature. 2006 Nov 16;444(7117):323-9
17108957
Evolution. 1999 Jun;53(3):704-716
28565630
Oecologia. 1997 Dec;113(1):133-139
28307288
Science. 2001 Jan 5;291(5501):118-20
11141561
Evolution. 1989 Jul;43(4):835-847
28564198
Mol Genet Genomics. 2010 Apr;283(4):305-15
20140455
Evolution. 2002 Jul;56(7):1340-51
12206236
Ecol Lett. 2008 Apr;11(4):327-37
18248450
Nature. 2001 Jun 14;411(6839):826-33
11459065
Trends Ecol Evol. 2008 Dec;23(12):678-85
18947899
Mol Ecol. 2008 Apr;17(7):1636-47
18266620
J Evol Biol. 2007 Nov;20(6):2371-8
17956398
Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:575-607
15012275
Genetics. 2001 Jul;158(3):1301-9
11454776
Evolution. 2006 Aug;60(8):1562-73
17017057