Search

Significance Root architecture is an important trait that is shaped by the formation of primary roots, lateral roots, and adventitious roots. Here, we show that three PLETHORA (PLT) transcription factors are the key molecular triggers for the de novo organ patterning during Arabidopsis lateral root formation. PLT3, PLT5, and PLT7 redundantly regulate the correct initiation of formative cell divisions in incipient lateral root primordia and the proper establishment of gene expression programs that lead to the formation of a new growth axis., Plant development is characterized by repeated initiation of meristems, regions of dividing cells that give rise to new organs. During lateral root (LR) formation, new LR meristems are specified to support the outgrowth of LRs along a new axis. The determination of the sequential events required to form this new growth axis has been hampered by redundant activities of key transcription factors. Here, we characterize the effects of three PLETHORA (PLT) transcription factors, PLT3, PLT5, and PLT7, during LR outgrowth. In plt3plt5plt7 triple mutants, the morphology of lateral root primordia (LRP), the auxin response gradient, and the expression of meristem/tissue identity markers are impaired from the “symmetry-breaking” periclinal cell divisions during the transition between stage I and stage II, wherein cells first acquire different identities in the proximodistal and radial axes. Particularly, PLT1, PLT2, and PLT4 genes that are typically expressed later than PLT3, PLT5, and PLT7 during LR outgrowth are not induced in the mutant primordia, rendering “PLT-null” LRP. Reintroduction of any PLT clade member in the mutant primordia completely restores layer identities at stage II and rescues mutant defects in meristem and tissue establishment. Therefore, all PLT genes can activate the formative cell divisions that lead to de novo meristem establishment and tissue patterning associated with a new growth axis.

Root systems can display variable architectures that contribute to survival strategies of plants. The model plant Arabidopsis thaliana possesses a tap root system, in which the primary root and lateral roots (LRs) are major architectural determinants. The phytohormone auxin fulfils multiple roles throughout LR development. In this review, we summarize recent advances in our understanding of four aspects of LR formation: (i) LR positioning, which determines the spatial distribution of lateral root primordia (LRP) and LRs along primary roots; (ii) LR initiation, encompassing the activation of nuclear migration in specified lateral root founder cells (LRFCs) up to the first asymmetric cell division; (iii) LR outgrowth, the 'primordium-intrinsic' patterning of de novo organ tissues and a meristem; and (iv) LR emergence, an interaction between LRP and overlaying tissues to allow passage through cell layers. We discuss how auxin signaling, embedded in a changing developmental context, plays important roles in all four phases. In addition, we discuss how rapid progress in gene network identification and analysis, modeling, and four-dimensional imaging techniques have led to an increasingly detailed understanding of the dynamic regulatory networks that control LR development.

Lateral roots (LRs), which originate from the growing root, and adventitious roots (ARs), which are formed from non-root organs, are the main contributors to the post-embryonic root system in Arabidopsis. However, our knowledge of how formation of the root system is altered in response to diverse inductive cues is limited. Here, we show that WOX11 contributes to root system plasticity. When seedlings are grown vertically on medium, WOX11 is not expressed in LR founder cells. During AR initiation, WOX11 is expressed in AR founder cells and activates LBD16. LBD16 also functions in LR formation and is activated in that context by ARF7/19 and not by WOX11. This indicates that divergent initial processes that lead to ARs and LRs may converge on a similar mechanism for primordium development. Furthermore, we demonstrated that when plants are grown in soil or upon wounding on medium, the primary root is able to produce both WOX11-mediated and non-WOX11-mediated roots. The discovery of WOX11-mediated root-derived roots reveals a previously uncharacterized pathway that confers plasticity during the generation of root system architecture in response to different inductive cues., Summary: Root system development can respond flexibly to developmental and environmental cues by utilizing WOX11-mediated and non-WOX11-mediated pathways, which converge on a common mechanism for primordium development involving LBD16.

Lateral roots (LRs), which originate from the growing root, and adventitious roots (ARs), which are formed from non-root organs, are main contributors to the post-embryonic root system in Arabidopsis. However, our knowledge of how the root system is plastically formed in response to diverse inductive cues is limited. Here we show that WOX11 contributes to root system plasticity. When seedlings are grown vertically on medium, WOX11 is not expressed in LR founder cells. During AR initiation, WOX11 is expressed in AR founder cells and activates LBD16. LBD16 also functions in LR formation and is activated in that context by ARF7/19 and not by WOX11. This indicates that divergent initial processes that lead to ARs and LRs may converge on the similar mechanism for primordium development. Furthermore, we demonstrated that when plants are grown in soil or upon wounding on medium, the primary root is able to produce both WOX11-mediated and non-WOX11-mediated roots. The discovery of WOX11-mediated root-derived roots reveals a previously uncharacterized pathway that confers plasticity during the generation of root system architecture in response to different inductive cues.

Lateral root primordia (LRP) originate from pericycle stem cells located deep within parental root tissues. LRP emerge through overlying root tissues by inducing auxin-dependent cell separation and hydraulic changes in adjacent cells. The auxin inducible auxin influx carrier LAX3 plays a key role concentrating this signal in cells overlying LRP. Delimiting LAX3 expression to two adjacent cell files overlying new LRP is critical to ensure auxin-regulated cell separation occurs solely along their shared walls. Multiscale modeling has predicted this highly focused pattern of expression requires auxin to sequentially induce auxin efflux and influx carriers PIN3 and LAX3, respectively. Consistent with model predictions, we report that LAX3 auxin inducible expression is regulated indirectly by the AUXIN RESPONSE FACTOR ARF7. Yeast-1-hybrid screens revealed the LAX3 promoter is bound by the transcription factor LBD29, which is a direct target for regulation by ARF7. Disrupting auxin inducible LBD29 expression or expressing an LBD29-SRDX transcriptional repressor phenocopied the lax3 mutant, resulting in delayed lateral root emergence. We conclude that sequential LBD29 and LAX3 induction by auxin is required to coordinate cell separation and organ emergence.

Background: The juxtaposition of newly formed primordia in the root and shoot differs greatly, but their formation in both contexts depends on local accumulation of the signaling molecule auxin. Whether the spacing of lateral roots along the main root and the arrangement of leaf primordia at the plant apex are controlled by related underlying mechanisms has remained unclear. Results: Here, we show that, in Arabidopsis thaliana, three transcriptional regulators implicated in phyllotaxis, PLETHORA3 (PLT3), PLT5, and PLT7, are expressed in incipient lateral root primordia where they are required for primordium development and lateral root emergence. Furthermore, all three PLT proteins prevent the formation of primordia close to one another, because, in their absence, successive lateral root primordia are frequently grouped in close longitudinal or radial clusters. The triple plt mutant phenotype is rescued by PLT-vYFP fusion proteins, which are expressed in the shoot meristem as well as the root, but not by expression of PLT7 in the shoot alone. Expression of all three PLT genes requires auxin response factors ARF7 and ARF19, and the reintroduction of PLT activity suffices to rescue lateral root formation in arf7,arf19. Conclusions: Intriguingly PLT 3, PLT5, and PLT7 not only control the positioning of organs at the shoot meristem but also in the root; a striking observation that raises many evolutionary questions.