Control of Arabidopsis lateral root primordium boundaries by <scp>MYB</scp>36

Fernández-Marcos, María; Desvoyes, Bénédicte; Manzano, Concepción; Liberman, Louisa M.; Benfey, Philip N.; Pozo, Juan C. del; Gutiérrez, Crisanto

doi:10.1111/nph.14304

Cited by 71 publications

(49 citation statements)

References 40 publications

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“…1F). This defect has also been observed in other mutants that specifically affect the emergence stage [9]. It is likely that initiation and/or founder cell specification stages are also disrupted to account for the full reduction in lateral root development.…”

Section: Resultssupporting

confidence: 56%

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Disruption of CYCLOPHILIN 38 function reveals a photosynthesis-dependent systemic signal controlling lateral root emergence

Duan

Pérez-Ruiz

Cejudo

et al. 2020

Preprint

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15Photosynthesis in leaves generates the fixed-carbon resources and essential 16 metabolites that support sink tissues, such as roots [1]. One of these products, sucrose, 17 is known to promote primary root growth, but it is not clear what other molecules may be 18 involved and whether other stages of root system development are affected by 19 photosynthate levels [2]. Through a mutant screen to identify pathways regulating root 20 system architecture, we identified a mutation in the CYCLOPHILIN 38 (CYP38) gene, 21 which causes an accumulation of pre-emergent stage lateral roots, with a minor effect on 22 primary root growth. CYP38 was previously reported to maintain the stability of 23 Photosystem II (PSII) in chloroplasts [3]. CYP38 expression is enriched in the shoot and 24 grafting experiments show that the gene acts non-cell autonomously to promote lateral 25 root emergence. Growth of wild-type plants under low light conditions phenocopied the 26 cyp38 lateral root emergence phenotype as did the inhibition of PSII-dependent electron 27 transport or NADPH production. Importantly, the cyp38 root phenotype is not rescued 28 by exogenous sucrose, suggesting the involvement of another metabolite. Auxin (IAA) is 29 an essential hormone promoting root growth and its biosynthesis from tryptophan is 30 dependent on reductant generated during photosynthesis [4,5]. Both WT seedlings 31 grown under low light and cyp38 mutants have highly diminished levels of IAA in root 32 tissues. The cyp38 lateral root defect is rescued by IAA treatment, revealing that 33 photosynthesis promotes lateral root emergence partly through IAA 34 biosynthesis. Metabolomic profiling shows that the accumulation of several defense-35 related metabolites are also photosynthesis-dependent, suggesting that the regulation of 36 a number of energy-intensive pathways are down-regulated when light becomes limiting. 37Results and Discussion: 38CYP38 is necessary for lateral root emergence 39 Lateral roots form through oriented cell divisions within the pericycle tissue layer, hidden 40 3-layers deep inside the parent root [6]. The process of lateral root primordia 41 emergence through these outer tissues involves communication between the organ identify the causative genetic locus, CYPLOPHILLIN 38 (CYP38) (Figure. S1B). A T-49 DNA allele (cyp38-5) with an insertion in the sixth exon phenocopied the EMS allele 50 (cyp38-4) (Figure. 1A-C), which has an early stop codon in the second exon (Figure.51 1D). Expression of CYP38 using its native promoter fully complement cyp38-4 (Figure.52 1E), indicating that CYP38 is indeed the causative gene. 54To determine the developmental basis for the cyp38 phenotype, we classified lateral root 55 growth into 4 distinct stages: initiation (I), pre-emergence (Pre-E), emergence (E), and 56 maturation (M) (Figure. S1A). Compared to wild type (WT), where the majority of lateral 57 roots have typically progressed to the maturation stage in 8-dpg (days post germination) 58 seedlings, we found that the cyp38-5 mutants had a si...

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Section: Resultssupporting

confidence: 56%

“…3J). ROS levels in lateral root primordia are important in regulating cell proliferation and differentiation in the primary root, and also facilitate the establishment of a dome shaped primordia [9]. Together, our observation suggests that the perturbed balance in chloroplast redox status may non-autonomously limit lateral root emergence.…”

Section: Resultsmentioning

confidence: 77%

Disruption of CYCLOPHILIN 38 function reveals a photosynthesis-dependent systemic signal controlling lateral root emergence

Duan

Pérez-Ruiz

Cejudo

et al. 2020

Preprint

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“…This emphasizes the importance of the direct control of FAMA/FLP by MUTE to achieve such coordination. Recently, the I1-FFL was implicated in transcriptional control of root Casparian strip differentiation (Fernandez-Marcos et al, 2017). Thus, plants may use I1-FFL for critical cell-fate decision-making processes in broader contexts.…”

Section: Discussionmentioning

confidence: 99%

MUTE Directly Orchestrates Cell State Switch and the Single Symmetric Division to Create Stomata

Han

Sugihara

et al. 2018

Preprint

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Highlights 22 23 •Complete inventories of gene expression in stomatal differentiation state are elucidated 24 •MUTE switches stomatal patterning program initiated by its sister bHLH, SPEECHLESS 25 •MUTE directly induces cell-cycle genes and their direct transcriptional repressors 26 •Incoherent feed-forward loop by MUTE ensures the single division of a stomatal 27 precursor 28 29 30 SUMMARY 31 Precise cell division control is critical for developmental patterning. For the differentiation of a 32 functional stoma, a cellular valve for efficient gas exchange, the single symmetric division of an 33 immediate precursor is absolutely essential. Yet, the mechanism governing the single division 34 event remains unclear. Here we report the complete inventories of gene expression by the 35 Arabidopsis bHLH protein MUTE, a potent inducer of stomatal differentiation. MUTE switches 36 the gene expression program initiated by its sister bHLH, SPEECHLESS. MUTE directly 37 induces a suite of cell-cycle genes, including CYCD5;1, and their transcriptional repressors, 38 FAMA and FOUR LIPS. The architecture of the regulatory network initiated by MUTE represents 39 an Incoherent Type 1 Feed-Forward Loop. Our mathematical modeling and experimental 40 perturbations support a notion that MUTE orchestrates a transcriptional cascade leading to the 41 tightly-restricted, robust pulse of cell-cycle gene expression, thereby ensuring the single cell 42 division to create functional stomata.43 44 93 lineage cells and singular GCs, respectively (MacAlister et al., 2007; Ohashi-Ito and Bergmann, 94 2006). We thus hypothesized that MUTE governs the gene regulatory networks to create 95 stomata. To test this, we performed a genome-wide profiling of early MUTE-responsive genes.96 5 Comparison of SPCH and MUTE target genes revealed how MUTE disconnects stomatal-97 lineage cells from extrinsic inhibitory signals, thus 'locks in' the differentiation program. Contrary 98 to the known role of MUTE in terminating the proliferating meristemoids (Pillitteri et al., 2007), 99 our study identified cell cycle and cell division genes as overwhelming majorities of the MUTE 100 targets. MUTE directly binds to the promoters and upregulates novel and previously described 101 cell-cycle regulators of the GMC symmetric division process. At the same time, MUTE directly 102 binds to the promoters and upregulates FAMA and FLP, which in turn repress the cell-cycle 103 regulators. Our mathematical modeling predictions and experimental perturbations of network 104 motif demonstrate that an incoherent feed-forward loop mediated by MUTE, cell cycle regulators, 105and FAMA/FLP is sufficient to articulate the single symmetric division event with high fidelity. 106Our study establishes the role for MUTE in orchestrating a transcriptional cascade leading to 107 stomatal differentiation and defines a core regulatory circuit for the single symmetric division. 108 109 Results 110 111 MUTE induces and represses specific sets of transcriptomes

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“…Moreover, MYB36 can directly bind to the upstream regulatory regions of CASPs and other CS-related genes [43], though this interaction likely requires a co-factor, which is also downstream of MYB36 [44]. Despite lacking a functional CS, myb36 mutants display a remarkably normal developmental phenotype with minor differences in root growth rate and length [43,44,47]. While the formation of CS is delayed, a barrier is eventually formed in more mature tissue [44] and there is overproduction of endodermal suberin [43].…”

Section: Myb36 Links Specification To Differentiationmentioning

confidence: 99%

Uncovering Gene Regulatory Networks Controlling Plant Cell Differentiation

2017

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The development of multicellular organisms relies on the precise regulation of cellular differentiation. As such, there has been significant effort invested to understand the process through which an immature cell undergoes differentiation. In this review, we highlight key discoveries and advances that have contributed to our understanding of the transcriptional networks underlying Arabidopsis root endodermal differentiation. To conclude, we propose perspectives on how advances in molecular biology, microscopy and nucleotide sequencing will provide the tools to test the biological significance of these gene regulatory networks.

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Control of Arabidopsis lateral root primordium boundaries by MYB36

Cited by 71 publications

References 40 publications

Disruption of CYCLOPHILIN 38 function reveals a photosynthesis-dependent systemic signal controlling lateral root emergence

Disruption of CYCLOPHILIN 38 function reveals a photosynthesis-dependent systemic signal controlling lateral root emergence

MUTE Directly Orchestrates Cell State Switch and the Single Symmetric Division to Create Stomata

Uncovering Gene Regulatory Networks Controlling Plant Cell Differentiation

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