The birth of a giant: evolutionary insights into the origin of auxin responses in plants

Abstract

The plant signaling molecule auxin is present in multiple kingdoms of life. Since its discovery, a century of research has been focused on its action as a phytohormone. In land plants, auxin regulates growth and development through transcriptional and non-transcriptional programs. Some of the molecular mechanisms underlying these responses are well understood, mainly in Arabidopsis. Recently, the availability of genomic and transcriptomic data of green lineages, together with phylogenetic inference, has provided the basis to reconstruct the evolutionary history of some components involved in auxin biology. In this review, we follow the evolutionary trajectory that allowed auxin to become the "giant" of plant biology by focusing on bryophytes and streptophyte algae. We consider auxin biosynthesis, transport, physiological, and molecular responses, as well as evidence supporting the role of auxin as a chemical messenger for communication within ecosystems. Finally, we emphasize that functional validation of predicted orthologs will shed light on the conserved properties of auxin biology among streptophytes.

Keywords: auxin; ecology; evolution; hormone response; plant biology.

Figure 1. Illustration of a land plant cell with the main components of auxin biology

The most common precursor of Indole 3‐acetic acid (IAA; indicated in orange structures) biosynthesis is tryptophan synthesized in the chloroplasts. In plants, indole‐3‐pyruvic acid (IPyA) is the major intermediate and this involves the function of TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) followed by decarboxylation catalyzed by members of the YUCCA (YUC) family. IAA can then be stored in the cells by forming amino acid conjugates catalyzed by GRETCHEN HAGEN3 (GH3) auxin‐amido synthetases. IAA is transported inside the cells via importers (AUX/LAX) or by diffusion (protonated form IAAH). IAA is an anionic form inside the cells and is exported via PIN proteins localized at the plasma membrane (PM). PILS is a family of proteins mainly localized to the endoplasmic reticulum (ER) and have an auxin‐transport function and presumably contribute to intracellular auxin homeostasis. A second family of PM transporters, ABCBs, act mainly as IAA efflux carriers, working together with PINs in transporting IAA outside the cells. Inside the nucleus, IAA regulates the NAP. When auxin is abundant in the nuclear environment (orange structures) it binds to members of the TIR1/AFB receptor family (light blue) part of a ubiquitin ligase complex and to AUX/IAA repressors (light blue), targeting the latter for degradation. Thus, the auxin response factors (ARFs) can activate the transcription of auxin‐responsive genes. AUXIN‐BINDING PROTEIN1 (ABP1) functions as auxin receptor in the apoplast, and it is known to mediate transmembrane kinase (TMK1) proteins that mediate rapid responses. TMK1 mediates the phosphorylation of AHA‐plasma membrane H⁺‐ATPases in the presence of auxin, which is translated into acidification of the apoplast.

Figure EV1. Phylogenetic tree of the TAA gene family with green algae and land plant homologs

Protein domains, Alliinase‐EGF and Alliinase‐C are indicated with “red” and “green” representations, respectively. TAR3/TAR4 clade shows the consistent presence of both domains in all lineages, whereas in TAA/TAR1/TAR2 clade, some phyla lack Alliinase‐EGF domain. Aminotransferases from land plants, other than TAA members, were used as outgroup sequences to root the tree. Branches that are well supported (bootstrap > 75) are indicated by green dots. Orthologs from each phylum are represented in different colors, as indicated in the right bottom right legend. Basic information about the tree construction: “software,” “model of evolution,” and the “number of taxa” used for phylogenetic tree construction are indicated at the center. The complete tree can be found at the interactive Tree of Life (iTOL) repository: https://itol.embl.de/shared/dolfweijers.

Figure EV2. Phylogenetic tree of the YUC gene family with algae and land plant homologs

The different FMO clades are indicated by representative Arabidopsis family member names (FMO, flavin monooxyenase 1; GS‐OX, FMO glucosinolate S‐oxygenase; N‐OX, FMO N‐oxygenases; YUC, Yucca). Branches that are well supported (bootstrap > 75) are indicated by green dots. Orthologs from each phylum are represented in different colors, as indicated in the bottom right legend. Basic information about the tree construction: “software,” “model of evolution,” and the “number of taxa” used for phylogenetic tree construction are indicated at the center. The complete tree can be found at the interactive Tree of Life (iTOL) repository: https://itol.embl.de/shared/dolfweijers.

Figure 2. Schematic summary of presence or absence of ancestral copies of the main genetic components of auxin biology in plants

Biosynthesis and metabolism (orange), transport (pink), transcriptional pathway (light blue), and non‐transcriptional regulation (purple). Orthologs present (blue circles) or absent (pink circles). Land plants also referred to as embryophytes (Embr.) are divided into tracheophytes and bryophytes and belong to the Viridiplantae (plants) clade of eukaryotic organisms. Plants are found in almost every habitat on Earth and are divided into two main clades, streptophytes and chlorophytes. The Streptophytes comprise a group of green algae, the streptophyte algae, and the land plants (One Thousand Plant Transcriptomes Initiative, 2019). Streptophyte algae are a paraphyletic group of extant algae that encompass the lower‐branching KCM‐grade classes, Klebsormidiophyceae, Chlorokybophyceae, and Mesostigmatophyceae and the higher‐branching ZCC‐grade classes, Zygnematophyceae, Coleochaetophyceae, and Charophyceae (de Vries & Archibald, 2018).

Figure EV3. Phylogenetic tree of the GH3 gene family with green algae and land plant homologs

Respective Arabidopsis orthologs that are present in the specific clade are mentioned with the corresponding Arabidopsis family member names. “Rest” includes GH3.7, 3.8, 3.12 until 3.19. Branches that are well supported (bootstrap > 75) are indicated by green dots. Orthologs from each phylum are represented in different colors, as indicated in the bottom right legend. Basic information about the tree construction: “software,” “model of evolution,” and the “number of taxa” used for phylogenetic tree construction are indicated at the center. The complete tree can be found at the interactive Tree of Life (iTOL) repository: https://itol.embl.de/shared/dolfweijers.

Figure 3. Evolutionary scenario of ancestral auxin biology in streptophytes

(A) Auxin (IAA) has been found in extant streptophyte algae and likely in the last common ancestor of streptophytes. However, the biosynthetic pathway for its production remains unknown. In streptophyte algae, there are predicted orthologs of gene families that in plants catalyze the conversion of Trp to IAA via IPyA, TAA, and YUC. Among the mechanisms that contribute to regulating IAA levels in plants, storage mediated by members of the GH3 gene family remains controversial in algae as only a few members of this family have been reported. Regarding transport (red), predicted orthologs of PIN, PILS, ABCB, and AUX/LAX are present in members of the green algae, suggesting that the transport function was present in an ancestral streptophyte. Several responses to auxin have been observed in streptophyte algae, but the mechanisms underlying these responses are unknown. In land plants, fast responses to auxin are mediated by auxin perception via the ABP1‐TMK1 module. In extant algae, the ABP1 gene family is well conserved, suggesting a plausible scenario in which an ancestral streptophyte might have been responding to local auxin produced in the phycosphere (red). (B) Homologs of the three main components of the NAP are present in extant algae. However, the TIR1‐like receptor and Aux/IAA‐like predicted orthologs lack the components to interact with auxin. Therefore, there is a plausible land plant scenario in which a diversified Proto‐ARF network came to be regulated by auxin upon innovations in TIR1 and Aux/IAA protein families.