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.

Multi-substrate specificity shaped the complex evolution of the aminotransferase family across the tree of life

“…1 C ). The 17 non-AT groups, which belong to AT classes but likely have non-AT activity (e.g., synthases, lyases, and other transferases), were still included in the analysis, as they improved the phylogenetic relationships of ATs ( Dataset S4 ), and some non-AT members can contain ATs, e.g., a Trp AT group found in the alliinases class 71 ( Fig. S7 ).…”

An auxin homeostat allows plant cells to establish and control defined transmembrane auxin gradients

“…In that, ABCB (and here not further discussed, ER-based PIN-LIKES, PILS; Feraru et al ., 2012) transporters are ancient auxin transporters and thus already exist in chlorophytes, while PINs — although they seem to appear in some chlorophytes (Skokan et al ., 2019; Carrillo-Carrasco et al ., 2023) — can be safely associated only with charophytic algae (Carrillo-Carrasco et al ., 2023). The origin of AUX1/LAXs, showing a more fragmentary distribution over charophytes and chlorophytes is less clear (Vosolsobě et al ., 2020; Geisler, 2021; Carrillo-Carrasco et al ., 2023).…”

“…In particular, the slow diffusion process hinders the rapid establishment of desired auxin gradients. In that respect it is worth mentioning that the early divergent charophyte algae Chlorokybus atmophyticus has ABCBs but apparently no PIN or AUX1/LAX (Vosolsobě et al ., 2020; Geisler, 2021; Carrillo-Carrasco et al ., 2023). The addition of AUX1/LAX was thus a major evolutionary event providing good homeostatic control overcoming the diffusion limit (case 2).…”

“…Another remarkable outcome of our modelling approach was that the apparent relevance of each transporter class for auxin homeostasis roughly recapitulates the current picture of auxin transporter evolution (Vosolsobě et al ., 2020; Geisler, 2021; Carrillo-Carrasco et al ., 2023). In that, ABCB (and here not further discussed, ER-based PIN-LIKES, PILS; Feraru et al ., 2012) transporters are ancient auxin transporters and thus already exist in chlorophytes, while PINs — although they seem to appear in some chlorophytes (Skokan et al ., 2019; Carrillo-Carrasco et al ., 2023) — can be safely associated only with charophytic algae (Carrillo-Carrasco et al ., 2023). The origin of AUX1/LAXs, showing a more fragmentary distribution over charophytes and chlorophytes is less clear (Vosolsobě et al ., 2020; Geisler, 2021; Carrillo-Carrasco et al ., 2023).…”

Analysis of auxin responses in the fernCeratopteris richardiiidentifies tissue ontogeny as a major determinant for response properties

“…Auxin, one of the most-studied and best-understood plant hormones, is crucial for many processes in bryophytes and tracheophytes (reviewed in (Kato et al, 2018)). The pathway mediating transcriptional auxin responses is conserved among all land plants and partly present in streptophyte algae (Carrillo-Carrasco et al, 2023; Mutte et al, 2018). Auxin controls many different developmental processes, including rhizoid formation in the bryophytes Marchantia and Physcomitrium (Flores-Sandoval et al, 2015; Sakakibara et al, 2003; Thelander et al, 2018) and root branching at the expense of root elongation in Arabidopsis (Casimiro et al, 2001; Dubrovsky et al, 2008; Lavenus et al, 2013).…”