Insights into the origin and evolution of the plant hormone signaling machinery

Abstract

Plant hormones modulate plant growth, development, and defense. However, many aspects of the origin and evolution of plant hormone signaling pathways remain obscure. Here, we use a comparative genomic and phylogenetic approach to investigate the origin and evolution of nine major plant hormone (abscisic acid, auxin, brassinosteroid, cytokinin, ethylene, gibberellin, jasmonate, salicylic acid, and strigolactone) signaling pathways. Our multispecies genome-wide analysis reveals that: (1) auxin, cytokinin, and strigolactone signaling pathways originated in charophyte lineages; (2) abscisic acid, jasmonate, and salicylic acid signaling pathways arose in the last common ancestor of land plants; (3) gibberellin signaling evolved after the divergence of bryophytes from land plants; (4) the canonical brassinosteroid signaling originated before the emergence of angiosperms but likely after the split of gymnosperms and angiosperms; and (5) the origin of the canonical ethylene signaling pathway postdates shortly the emergence of angiosperms. Our findings might have important implications in understanding the molecular mechanisms underlying the emergence of land plants.

Figure 1.

Schematic diagrams of nine major plant hormone signaling pathways: AUX signaling (A), JA signaling (B), GA signaling (C), SL signaling (D), CK signaling (E), BR signaling (F), ETH signaling (G), ABA signaling (H), and SA signaling (I). For detailed molecular mechanisms, see the introduction. ER, Endoplasmic reticulum; NM, nuclear membrane.

Figure 2.

The distribution of plant hormone signaling components in plants. The rings and solid circles indicate the presence of homologs and orthologs, respectively. Superscript 1 indicates that a significant hit can be gained by similarity searches using the P. patens proteins as BLAST queries. Protein names in blue and purple indicate these mediating plant hormone signal transduction and transport, respectively. Columns in green and light blue indicate genome sequences and transcriptome data used for similarity searches, respectively.

Figure 3.

The origin of nine major plant hormone signaling pathways in plants. The green bars indicate the emergence of all the components of each specific hormone signaling machinery. Branches in blue and purple indicate algae and land plants, respectively. The phylogenetic relationship among the plant species used in this study is based on Qiu et al. (2006), Finet et al. (2010), and Bowman (2013).

Figure 4.

The phylogenetic relationship of the CHASE domains of prokaryotic and eukaryotic origin. The phylogeny is an approximate maximum-likelihood (ML) tree reconstructed using FastTree 2 based on the CHASE domain sequences of both prokaryotes and eukaryotes. SH-like values are shown near selected nodes.

Figure 5.

The phylogenetic relationship and domain architecture of SA receptors. The phylogeny is an ML tree reconstructed based on homologs of SA receptors, NPRs. Bootstrap values (ML/neighbor-joining) are shown near the nodes. Domain architecture was mapped near the protein. Different domains are represented by rectangles with different colors.

Figure 6.

The phylogenetic relationship and domain architecture of JA and AUX receptors. The phylogeny is an ML tree reconstructed based on homologs of JA and AUX receptors. Bootstrap values (ML/neighbor-joining) are shown near the nodes. Domain architecture was mapped near the protein. Different domains are represented by rectangles with different colors. Protein structures of JA and AUX receptor orthologs are shown near the corresponding proteins.