The evolution of plant nuclear genes

Abstract

We analyze the evolutionary dynamics of three of the best-studied plant nuclear multigene families. The data analyzed derive from the genes that encode the small subunit of ribulose-1,5-bisphosphate carboxylase (rbcS), the gene family that encodes the enzyme chalcone synthase (Chs), and the gene family that encodes alcohol dehydrogenases (Adh). In addition, we consider the limited evolutionary data available on plant transposable elements. New Chs and rbcS genes appear to be recruited at about 10 times the rate estimated for Adh genes, and this is correlated with a much smaller average gene family size for Adh genes. In addition, duplication and divergence in function appears to be relatively common for Chs genes in flowering plant evolution. Analyses of synonymous nucleotide substitution rates for Adh genes in monocots reject a linear relationship with clock time. Replacement substitution rates vary with time in a complex fashion, which suggests that adaptive evolution has played an important role in driving divergence following gene duplication events. Molecular population genetic studies of Adh and Chs genes reveal high levels of molecular diversity within species. These studies also reveal that inter- and intralocus recombination are important forces in the generation allelic novelties. Moreover, illegitimate recombination events appear to be an important factor in transposable element loss in plants. When we consider the recruitment and loss of new gene copies, the generation of allelic diversity within plant species, and ectopic exchange among transposable elements, we conclude that recombination is a pervasive force at all levels of plant evolution.

Figure 1

A neighbor-joining tree depicting the relationships of the mature gene products of rbcS. The data were taken from GenBank subject to the following restrictions. (i) Only sequences that differed by 5% or more in primary nucleotide sequence were incorporated in the analysis to avoid the inclusion of allelic sequences. (ii) Only sequences that represented a minimum of 50% of the gene were included to avoid biases associated with very short sequences. Amino acid sequences were aligned and the neighbor-joining tree (20) was constructed based on corrected distances (21) using the program clustal w (22).

Figure 2

Anthocyanin and flavonol biosynthetic pathway. The enzymes in bold represent the core genes of flavonoid biosynthesis. PAL, phenylalanine ammonia-lyase; C4H, cinnamate 4-hydroxylase; 4CL, 4-coumarate-coenzyme A ligase; CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone 3-hydroxylase; F3′H, flavonoid 3′-hydroxylase; F3′5′H, flavonoid 3′5′-hydroxylase; DFR, dihydroflavonol 4-reductase; AS, anthocyanidin synthase; UF3GT, UDP-glucose flavonoid 3-oxy-glucosyl transferase; RT, rhamnosyl transferase. Also shown within the box associated with enzyme designations are the gene super families from which particular enzymes are thought to be derived.

Figure 3

Regulation of the anthocyanin pathway in two dicot species. (Asterisks denote genes for which clones have been made from Ipomoea.) The regulatory genes that have been identified in Antirrhinum and Petunia are shown along with the genes that they regulate. Abbreviations are listed in the legend for Fig. 2.

Figure 4

Neighbor-joining tree depicting the relationships of ADH amino acid sequences. The data selection criteria and analytical methods are the same as those described for Fig. 1.