Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus

Abstract

Glucosinolate profiles differ among Arabidopsis thaliana ecotypes, caused by the composition of alleles at several glucosinolate biosynthetic loci. One of these, GS-Elong, harbors a family of methylthioalkylmalate synthase (MAM) genes that determine the side chain length of aliphatic glucosinolate structures. Fine mapping reveals that GS-Elong constitutes an insect resistance quantitative trait locus, caused by variation in glucosinolate profiles conferred by polymorphism of MAM alleles in this region. A sequence survey of randomly chosen ecotypes indicates that GS-Elong is highly variable among A. thaliana ecotypes: indel polymorphisms are frequent, as well as gene conversion events between gene copies arranged in tandem. Furthermore, statistical methods of molecular population genetics suggest that one of the genes, MAM2, is subject to balancing selection. This may be caused by ecological tradeoffs, i.e., by contrasting physiological effects of glucosinolates on generalist vs. specialist insects.

Fig. 1.

GS-Elong region in A. thaliana ecotypes. Maximal levels of divergence between MAM1 and MAM2 (nearly 5%) occur in the Sorbo ecotype, which likely represents the ancestral gene arrangement. Genes are patterned as most similar to Sorbo MAM1 (vertically patterned) or Sorbo MAM2 (horizontally patterned). Triangles indicate large deletions. Predominant glucosinolate side chain length is indicated on the right: glucosinolates with four methylene groups (4, e.g., Col-0) or three methylene groups (3, e.g., Ler-0). Notice that synthesis of C₄ glucosinolates is completely associated with occurrence of a full-length Sorbo-like MAM1 gene. Otherwise, C₃ glucosinolates are synthesized.

Fig. 2.

Sliding window analysis of nucleotide polymorphism (π) among MAM1 and MAM2 genes. Arrows indicate regions where compared sequences are identical because of one or more presumptive gene conversion events between paralogous genes. The peaks between 500 and 590 and between 1,820 and 1,830 nucleotides stem from complex changes resulting in poor sequence alignment. (A) All sampled MAM1 and MAM2 alleles (except truncated alleles). (B) MAM1 versus MAM2 in the Condara ecotype. Differences between MAM1 and MAM2 are very similar in Hodja. (C) MAM1 versus MAM2 in the Sorbo ecotype. (D) MAM1 versus MAM2 in the Cvi-0 ecotype. (E) MAM1 versus MAM2 in the Cal-0 ecotype. (F) MAM1 versus MAM2 in the Mr-0 ecotype. Window size, 50 nt; step width: 10 nt. Alignment gaps are included in scaling of the horizontal axis. The MAM gene structure is depicted above the panels.

Fig. 3.

Quantitative effects in near-isogenic lines carrying the Col-0 MAM1 (white bars) or the Ler-0 MAM2 allele (gray bars) at GS-Elong. Data are least square means (± standard error) from ANOVA (Col-0 = 100) for growth rate (GR), total aliphatic glucosinolates (GS), damage by S. exigua (S.e.), and by P. xylostella (P.x.). ***, P < 0.001.

Fig. 4.

QTL mapping of total leaf glucosinolate content (dashed line) and resistance to S. exigua (solid line). Statistical significance is indicated by F ratios.