Evolution of auxin signaling
From Purdue Genomics Database Facility
Cédric Finet (cedric.finet@ens-lyon.org) / Michael Prigge (mprigge@indiana.edu)
Evolutionary overview of auxin signaling (gene content)
This part of our work is complementary to the vignette "auxin" posted by N. Shinohara, Y. Hiwatashi, T. Aoyama, N. Aono, T. Hirai, and T. Nishiyama. Our results are summarized in the file AuxinGeneWorkbook.xls available at the following website : [1].
Gene family members were identified following BLAST searches of the Physcomitrella protein (JGI V1.1) and/or nucleotide databases, the 11/10/06 assembly of the Selaginella genome (http://selaginella.genomics.purdue.edu/), as well as the most recent protein datasets for Arabidopsis (TAIR v6), rice (TIGR v4), and Populus (JGI v1.1). The numbers of gene family members were revised based on the topologies of Bayesian-inferred phylogenetic trees from amino-acid alignments.
The number of genes in the ancestral land plant, the ancestral vascular plant, and the ancestral angiosperm refer specifically to the last common ancestor of moss and vascular plants, of Selaginella and angiosperms, and of monocot and eudicot angiosperms.
The Nitrilase proteins likely involved in auxin synthesis from maize and Arabidopsis are polyphyletic, so it unclear whether indole-3-acetonitrilase activity reflects the ancestral function or a more recently derived function.
The most similar moss proteins do not group within or directly sister to the vascular plant genes implicated in auxin homeostasis.
Appearance of GH3-class II genes in the lineage leading to lycophytes
The GH3-class II family is one of the three major classes of early auxin reponse genes identified in plants: Aux/IAA, SAUR and GH3 (Abel and Theologis, 1996). Contrary to the Aux/IAA and SAUR genes, the GH3-class II genes are absent from the genome of Physcomitrella patens. But this lineage appears in the genome of Selaginella moellendorfii with the gene e_gw1.28.432.1 that I annotated as a GH3-class II gene. This ancestral lineage will lead to extant genes GH3.1, GH3.2, GH3.3, GH3.4, GH3.5 an GH3.6 known in Arabidopsis thaliana. The GH3-class II family is really exciting if we discuss its appearance in an "evo-devo" context. For instance, the GH3.6 (DFL1) and GH3.2 (YDK1) and mutants harbour a short primary root, a reduced lateral root number, and reduced apical dominance (Nakazawa et al. 2001, Takase et al. 2004). Thus we can point out an interesting correlation between root innovations in lycophytes and the appearance of the GH3-class II family.
The phylogenetic tree (and the alignment) of the GH3 family is available at the following URL : [2], [3] and [4].
Diversification of IAA conjugates by appearance of new enzymes in lycophytes
(i) We can distinguish several key IAA-amino acid amidohydrolases involved in IAA conjugation / hydrolysis in Arabidopsis thaliana :
- a first phylogenetic unit with ILL3 and ILR1 genes ; ILR1 is known to provide free IAA by hydrolysing IAA-Leucine (Bartel and Fink, 1995)
- a second phylogenetic unit with ILL1/2/5/6 and IAR3 genes ; IAR3 is known to provide free IAA by hydrolysing IAA-Alanine (Davies et al. 1999)
As it has been previously shown (Rensing et al. 2008), the lineage leading to ILL3 / ILR1 was already present in bryophytes (and so forth in lycophytes). Surprinsingly, the genes leading to the ILL1/2/5/6 / IAR3 lineage appeared in lycophytes (gene fgenesh2_pg.C_scaffold_10000357 in Selaginella). In the light of these preliminary results, we can hypothesize that the regulation of the level of free IAA in the cell by the conjugation/hydrolysis became more and more important during evolution. These genomic data confirm some physiological data obtained by Cooke et al. (2002).
(ii) Additionally, there are no orthologues of the gene coding for IAMT1 (IAA-methyltransferase) in bryophytes nor in Selaginella moeellendorfii. IAMT1 is involved in the conjugation of IAA into MelAA in Arabidopsis thaliana and interestingly, this gene is necessary in the establishment of abaxial/adaxial polarity in lateral organs (Qin et al. 2005). This enzyme appeared after the divergence of lycophytes. Here a very exciting correlation between the establishment of a new way of regulation of auxin signaling and the establishment of abaxial/adaxial polarity during evolution. At this point it would be interesting to see what about other genes involved in polarity (HD-ZIP III, ...).
The phylogenetic tree (and the alignment) of the GH3 family is available at the following URL : [5] and [6].
Diversification of Aux/IAA family after the speciation of lycophytes
The Aux/IAA family is an huge family in angiosperms with 29 members in Arabidopsis (Liscum and Reed, 2002) and 35 members in Populus (Kalluri et al., 2007). In gymnosperms, at least 5 Aux/IAA genes are present as it has been shown in Pinus taeda (Goldfarb et al., 2003). Surprinsingly, only 3 and 4 Aux/IAA genes are respectively present in Physcomitrella and Selaginella. We could hypothesize that the number of Aux/IAA genes is proportional to the number of ARF genes as it is the case in angiosperms, but it does not seem to be the case in basal lineages in which the number of ARFs is intermediate and the number of Aux/IAAs very low. The diversification of Aux/IAA family could have been responsible for innovations in spermaphytes but not in bryophytes and lycophytes.
Our results (and therefore the genome of the spikemoss) challenge a recent review on the evolution of auxin signaling
A recent review published in The Plant Cell (Lau et al., 2008) claims that the ARF, Aux/IAA gene families and the auxin receptor(s) are absent from the lycophytes. Of course, our results demonstrate that these families are present in Selaginella genome.
Annotated proteins
ID 103740 ID 99818 ID 421726 ID 178850 ID 170974 ID 449292 ID 36236 ID 25877 ID 18600 ID 18617 ID 61687 ID 61688 ID 51694 ID 51695
References
Abel S, Theologis A. 1996. Early genes and auxin action. Plant Physiology 111 : 9-17.
Bartel B, Fink GR. 1995. ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268 : 1745-48.
Cooke TJ, Poli D, Sztein AE, Cohen JD. 2002. Evolutionary patterns in auxin action. Plant Molecular Biology 49 : 319-338.
Davies RT, Goetz DH, Lasswell J, Anderson MN, Bartel B. 1999. IAR3 encodes an auxin conjugate hydrolase from Arabidopsis. The Plant Cell 11(3) : 365-76.
Goldfarb B, Lanz-Garcia C, Lian Z, Whetten R. 2003. Aux/IAA gene family is conserved in the gymnosperm, loblolly pine (Pinus taeda). Tree Physiology 23(17) : 1181-92.
Kalluri UC, DiFazio SP, Brunner AM, Tuskan GA. 2007. Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biology 7 : 59.
Lau S, Jurgens G, De Smet I. 2008. The evolving complexity of the auxin pathway. The Plant Cell (preview online publication).
Liscum E, Reed JW. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Molecular Biology 49 : 387-400.
Nakazawa M, Yabe N, Ichikawa T, Yamamoto YY, Yoshizumi T, Hasunuma K, Matsui M. 2001. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, an positively regulates the light response of hypocotyl length. The Plant Journal 25(2) : 213-21.
Rensing et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319 : 64-69.
Qin G, Gu H, Zhau Y, Ma Z, Shi G, Yang Y, Pichersky E, Chen H, Liu M, Chen Z, Qu LJ. 2005. An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. The Plant cell 17(10) : 2693-704.
Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M. 2004. ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. The Plant Journal, 37(4), 471-83.
