Conservation of <i>Lotus</i> and Arabidopsis Basic Helix-Loop-Helix Proteins Reveals New Players in Root Hair Development

Karas, Bogumil J.; Amyot, Lisa; Johansen, Christopher T.; Sato, Shusei; Tabata, Satoshi; Kawaguchi, Masayoshi; Szczygłowski, Krzysztof

doi:10.1104/pp.109.143867

Cited by 111 publications

(114 citation statements)

References 36 publications

Supporting

Mentioning

109

Contrasting

Unclassified

Order By: Relevance

“…However, although we showed that the genetic components of this gene-regulatory network have been conserved, the detailed patterns of transcriptional regulation within this network remain to be resolved. For example, AtRHD6 and AtRSL1 (class I RSL genes) regulate the expression of AtLRL3 in A. thaliana (13,14), but we could not find evidence that PpRSL genes control PpLRL gene expression in P. patens. If there is a genuine absence of transcriptional regulation between LRL and class I RSL genes in P. patens, then two alternative evolutionary scenarios can be suggested.…”

Section: Discussioncontrasting

confidence: 67%

“…We show here that LRL genes positively regulate the development of the tip-growing rhizoids and caulonema in the moss P. patens. LRL genes also positively regulate the development of root hairs in angiosperms (13)(14)(15). Given that similar proteins control the development of filamentous rooting cells at the plant-soil interface in mosses and angiosperms, we conclude that LRL genes positively regulated the development of tip-growing rooting cells in the common ancestor of mosses and angiosperms that existed sometime before 420 y ago (30).…”

Section: Discussionmentioning

confidence: 72%

“…The group VIII basic helix-loop-helix transcription factors, AtROOT HAIR DEFECTIVE6 (AtRHD6) and AtROOT HAIR DEFECTIVE6-LIKE1 (AtRSL1), promote the development of root hairs by positively regulating AtLRL3 expression (13,14). To determine whether there are regulatory interactions between PpRSL and PpLRL genes, we compared the expression of PpLRL1 and PpLRL2 in Pprsl1 Pprsl2 double mutants and WT, and the expression of PpRSL1 and PpRSL2 in Pplrl1 Pplrl2 double mutants with WT.…”

Section: Significancementioning

confidence: 99%

“…Group XI bHLH transcription factors encoded by LOTUS JAPONICUS ROOTHAIRLESS1-LIKE (LRL) genes are also key regulators of root-hair development in angiosperms. LRL genes encode several proteins that regulate root-hair development in diverse angiosperms, including ROOTHAIRLESS1 (LjRHL1) in Lotus japonicus, AtLRL1, AtLRL2, AtLRL3 in A. thaliana (13,14), and ROOTHAIRLESS1 (OsRHL1) in Oryza sativa (15). Other LRL genes include OsPTF1, involved in phosphate starvation tolerance in rice (16), and AtUNE12, involved in female gametophyte development in Arabidopsis (17).…”

mentioning

confidence: 99%

See 3 more Smart Citations

Conserved regulatory mechanism controls the development of cells with rooting functions in land plants

Tam

Catarino

Dolan

2015

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Land plants develop filamentous cells-root hairs, rhizoids, and caulonemata-at the interface with the soil. Members of the group XI basic helix-loop-helix (bHLH) transcription factors encoded by LOTUS JAPONICUS ROOTHAIRLESS1-LIKE (LRL) genes positively regulate the development of root hairs in the angiosperms Lotus japonicus, Arabidopsis thaliana, and rice (Oryza sativa). Here we show that auxin promotes rhizoid and caulonema development by positively regulating the expression of PpLRL1 and PpLRL2, the two LRL genes in the Physcomitrella patens genome. Although the group VIII bHLH proteins, AtROOT HAIR DEFECTIVE6 and AtROOT HAIR DEFECTIVE SIX-LIKE1, promote roothair development by positively regulating the expression of AtLRL3 in A. thaliana, LRL genes promote rhizoid development independently of PpROOT HAIR DEFECTIVE SIX-LIKE1 and PpROOT HAIR DEFECITVE SIX-LIKE2 (PpRSL1 and PpRSL2) gene function in P. patens. Together, these data demonstrate that both LRL and RSL genes are components of an ancient auxin-regulated gene network that controls the development of tip-growing cells with rooting functions among most extant land plants. Although this network has diverged in the moss and the angiosperm lineages, our data demonstrate that the core network acted in the last common ancestor of the mosses and angiosperms that existed sometime before 420 million years ago.auxin | bHLH | evolution | rhizoids | root hairs T he evolution of rooting structures was a key morphological innovation that occurred when plants colonized the relatively dry continental surfaces of the planet sometime before 470 million year ago. The rooting structures of the earliest diverging groups of land plants comprised systems of rhizoids. Rhizoids are either unicellular filaments (in liverworts and hornworts) or multicellular (in mosses) and elongate into the growth substrate or air surrounding the plant. Bryophyte (liverwort, moss, and hornwort) rhizoids develop on gametophytes, the multicellular haploid stage in the life cycle. The evolution of vascular plants was accompanied by an increase in the morphological diversity of the sporophyte, the diploid multicellular stage of the plant life cycle (1). Roots, multicellular axes derived from meristems with protective caps, were a key innovation that first appeared in the fossil record ∼380 million years ago and likely evolved at least twice-at least once among the Lycophytes and at least once in the Euphyllophyte clade (2). Roots generally grow into the soil and expand the plant-soil interface into different soil horizons. For example, some root systems extend deep into the soil (taproots), whereas others proliferate in the nutrient-rich horizons near the soil surface. However, unicellular, filamentous protuberances called root hairs, which are morphologically similar to rhizoids, develop on all roots with few exceptions (2-5). Despite the different contexts in which they develop, root hairs and rhizoids carry out similar rooting functions, including nutrient uptake and anchorage (6, 7).Group VIII b...

show abstract

Section: Discussioncontrasting

confidence: 67%

Section: Discussionmentioning

confidence: 72%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Conserved regulatory mechanism controls the development of cells with rooting functions in land plants

Tam

Catarino

Dolan

2015

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…PIF-like genes in P. patens also lack the APB motif but contain a putative APA motif (Supplemental Figure 10), suggesting that the APB motif might have been acquired during the course of land plant evolution. The M. polymorpha protein most similar to Mp-PIF, Mapoly0502s0001, was placed in another clade, subfamily XI (Pires and Dolan, 2010), together with At-LRL1, which functions in root hair development (Karas et al, 2009). Neither the APA nor the APB motifs are present in the sequences of the proteins in subfamily XI, supporting the notion that M. polymorpha has only a single PIF transcription factor.…”

Section: Polymorpha Has a Single Pif Transcription Factormentioning

confidence: 55%

Phytochrome Signaling Is Mediated by PHYTOCHROME INTERACTING FACTOR in the Liverwort Marchantia polymorpha

et al. 2016

View full text Add to dashboard Cite

ORCID ID: 0000-0003-0504-8196 (K. Ishizaki)Phytochromes are red light (R) and far-red light (FR) receptors that play important roles in many aspects of plant growth and development. Phytochromes mainly function in the nucleus and regulate sets of genes by inhibiting negatively acting basic helix-loop-helix transcription factors named PHYTOCHROME INTERACTING FACTORs (PIFs) in Arabidopsis thaliana. Although R/FR photoreversible responses and phytochrome genes are well documented in diverse lineages of plants, the extent to which phytochrome signaling is mediated by gene regulation beyond angiosperms remains largely unclear. Here, we show that the liverwort Marchantia polymorpha, an emerging model basal land plant, has only one phytochrome gene, Mp-PHY, and only one PIF gene, Mp-PIF. These genes mediate typical low fluence responses, which are reversibly elicited by R and FR, and regulate gene expression. Mp-phy is light-stable and translocates into the nucleus upon irradiation with either R or FR, demonstrating that the single phytochrome Mp-phy exhibits combined biochemical and cell-biological characteristics of type I and type II phytochromes. Mp-phy photoreversibly regulates gemma germination and downstream gene expression by interacting with Mp-PIF and targeting it for degradation in an R-dependent manner. Our findings suggest that the molecular mechanisms for light-dependent transcriptional regulation mediated by PIF transcription factors were established early in land plant evolution.

show abstract

Overexpression of AHL proteins enhances root hair production by altering the transcription of RHD6‐downstream genes

et al. 2023

View full text Add to dashboard Cite

AT‐HOOK MOTIF NUCLEAR LOCALIZED (AHL) proteins occur in all sequenced plant species. They bind to the AT‐rich DNA sequences in chromosomes and regulate gene transcription related to diverse biological processes. However, the molecular mechanism underlying how AHL proteins regulate gene transcription is poorly understood. In this research, we used root hair production as a readout to study the function of two Arabidopsis AHL proteins, AHL17, and its closest homolog AHL28. Overexpression of AHL17 or AHL28 greatly enhanced root hair production by increasing the transcription of an array of genes downstream of RHD6. RHD6 is a key transcription factor that regulates root hair development. Mutation of RHD6 completely suppressed the overproduction of root hairs by blocking the transcription of AHL17‐activated genes. The overexpression of AHL17 or AHL28, however, neither affected the transcription of RHD6 nor the accumulation of RHD6 protein. These two AHL proteins also did not directly interact with RHD6. Furthermore, we found that three members of the Heat Shock Protein70 family, which have been annotated as the subunits of the plant Mediator complex, could form a complex with both AHL17 and RHD6. Our research might reveal a previously unrecognized mechanism of how AHL proteins regulate gene transcription.

show abstract

Conservation of Lotus and Arabidopsis Basic Helix-Loop-Helix Proteins Reveals New Players in Root Hair Development

Cited by 111 publications

References 36 publications

Conserved regulatory mechanism controls the development of cells with rooting functions in land plants

Conserved regulatory mechanism controls the development of cells with rooting functions in land plants

Phytochrome Signaling Is Mediated by PHYTOCHROME INTERACTING FACTOR in the Liverwort Marchantia polymorpha

Overexpression of AHL proteins enhances root hair production by altering the transcription of RHD6‐downstream genes

Contact Info

Product

Resources

About