Plants have evolved sophisticated root systems that help them to cope with harsh environmental conditions. They are typically composed of a primary root and lateral roots (LRs), but may also include adventitious roots (ARs). Unlike LRs, ARs may be initiated not only from pericycle cells, but from various cell types and tissues depending on the species. Phytohormones, together with many other internal and external stimuli, coordinate and guide every step of AR formation from the first event of cell reprogramming until emergence and outgrowth. In this review, we summarize recent advances in the molecular mechanisms controlling AR formation and highlight the main hormonal cross talk involved in its regulation under different conditions and in different model systems.

Summary: Adventitious root initiation (ARI) is a de novo organogenesis program and a key adaptive trait in plants. Several hormones regulate ARI but the underlying genetic architecture that integrates the hormonal crosstalk governing this process remains largely elusive. In this study, we use genetics, genome editing, transcriptomics, hormone profiling and cell biological approaches to demonstrate a crucial role played by the APETALA2/ETHYLENE RESPONSE FACTOR 115 transcription factor. We demonstrate that ERF115 functions as a repressor of ARI by activating the cytokinin (CK) signaling machinery. We also demonstrate that ERF115 is transcriptionally activated by jasmonate (JA), an oxylipin‐derived phytohormone, which represses ARI in NINJA‐dependent and independent manners. Our data indicate that NINJA‐dependent JA signaling in pericycle cells blocks early events of ARI. Altogether, our results reveal a previously unreported molecular network involving cooperative crosstalk between JA and CK machineries that represses ARI.

Adventitious rooting is a post-embryonic developmental program governed by a multitude of endogenous and environmental cues. Auxin, along with other phytohormones, integrates and translates these cues into precise molecular signatures to provide a coherent developmental output. Auxin signaling guides every step of adventitious root (AR) development from the early event of cell reprogramming and identity transitions until emergence. We have previously shown that auxin signaling controls the early events of AR initiation (ARI) by modulating the homeostasis of the negative regulator jasmonate (JA). Although considerable knowledge has been acquired about the role of auxin and JA in ARI, the genetic components acting downstream of JA signaling and the mechanistic basis controlling the interaction between these two hormones are not well understood. Here we provide evidence that COI1-dependent JA signaling controls the expression of DAO1 and its closely related paralog DAO2. In addition, we show that the dao1-1 loss of function mutant produces more ARs than the wild type, probably due to its deficiency in accumulating JA and its bioactive metabolite JA-Ile. Together, our data indicate that DAO1 controls a sensitive feedback circuit that stabilizes the auxin and JA crosstalk during ARI.

Vegetative propagation relies on the capacity of plants to regenerate de novo adventitious roots (ARs), a quantitative trait controlled by the interaction of endogenous factors, such as hormones and environmental cues among which light plays a central role. However, the physiological and molecular components mediating light cues during AR initiation (ARI) remain largely elusive. Here, we explored the role of red light (RL) on ARI in de-rooted Norway spruce seedlings. We combined investigation of hormone metabolism and gene expression analysis to identify potential signaling pathways. We also performed extensive anatomical characterization to investigate ARI at the cellular level. We showed that in contrast to white light, red light promoted ARI likely by reducing jasmonate (JA) and JA-isoleucine biosynthesis and repressing the accumulation of isopentyl-adenine-type cytokinins. We demonstrated that exogenously applied JA and/or CK inhibit ARI in a dose-dependent manner and found that they possibly act in the same pathway. The negative effect of JA on ARI was confirmed at the histological level. We showed that JA represses the early events of ARI. In conclusion, RL promotes ARI by repressing the accumulation of the wound-induced phytohormones JA and CK.

Adventitious rooting is a de novo organogenesis process that enables plants to propagate clonally and cope with environmental stresses. Adventitious root initiation (ARI) is controlled by interconnected transcriptional and hormonal networks, but there is little knowledge of the genetic and molecular programs orchestrating these networks. Thus, we have applied genome-wide transcriptome profiling to elucidate the transcriptional reprogramming events preceding ARI. These reprogramming events are associated with the down-regulation of cytokinin (CK) signaling and response genes, which could be triggers for ARI. Interestingly, we found that CK free base (iP, tZ, cZ, and DHZ) content declined during ARI, due to down-regulation of de novo CK biosynthesis and up-regulation of CK inactivation pathways. We also found that MYC2-dependent jasmonate (JA) signaling inhibits ARI by down-regulating the expression of the CYTOKININ OXIDASE/DEHYDROGENASE1 (CKX1) gene. We also demonstrated that JA and CK synergistically activate expression of the transcription factor RELATED to APETALA2.6 LIKE (RAP2.6L), and constitutive expression of this transcription factor strongly inhibits ARI. Collectively, our findings reveal that previously unknown genetic interactions between JA and CK play key roles in ARI.