HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers

Zhou, Yun; An, Yan; Han, Han; Li, Ting; Geng, Yichao; Liu, Xing; Meyerowitz, Elliot M.

doi:10.1126/science.aar8638

Cited by 124 publications

(178 citation statements)

References 34 publications

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“…In the model plant Arabidopsis, several key pathways in control of stem cell homeostasis in the SAMs have been identified [2][3][4] . Among them, the HAIRY MERISTEM (HAM) family GRAS (GAI, RGA and SCR) domain transcription factors play essential roles in determining the specification and proliferation of stem cells in the SAMs [4][5][6][7][8][9] . Two HAM family members, HAM1 and HAM2 proteins, interact with the homeodomain transcription factor WUSCHEL (WUS) and function together with WUS to regulate downstream gene expression and maintain the stem cell homeostasis 7,8 .…”

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confidence: 99%

“…Two HAM family members, HAM1 and HAM2 proteins, interact with the homeodomain transcription factor WUSCHEL (WUS) and function together with WUS to regulate downstream gene expression and maintain the stem cell homeostasis 7,8 . In addition, HAM1 and HAM2 keep the CLV3 expression off at the inner cell layers to establish an apical-basal polarity of the SAMs and the de novo axillary stem cell niches 9,10 . Through both computational modeling and experimentation, we previously found that HAM1/2 are expressed with a concentration gradient from the epidermis to the deep cell layers in the SAMs, which is important for the stem cell homeostasis in the established SAM 9 .…”

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A signal cascade originated from epidermis defines apical-basal patterning of Arabidopsis shoot apical meristems

Han

et al. 2020

Nat Commun

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In multicellular organisms, a long-standing question is how spatial patterns of distinct cell types are initiated and maintained during continuous cell division and proliferation. Along the vertical axis of plant shoot apical meristems (SAMs), stem cells are located at the top while cells specifying the stem cells are located more basally, forming a robust apical-basal pattern. We previously found that in Arabidopsis SAMs, the HAIRY MERISTEM (HAM) family transcription factors form a concentration gradient from the epidermis to the interior cell layers, and this gradient is essential for the stem cell specification and the apical-basal patterning of the SAMs. Here, we uncover that epidermis specific transcription factors, ARABIDOPSIS THALIANA MERISTEM LAYER 1 (ATML1) and its close homolog, define the concentration gradient of HAM in the SAM through activating a group of microRNAs. This study provides a molecular framework linking the epidermis-derived signal to the stem cell homeostasis in plants.

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A signal cascade originated from epidermis defines apical-basal patterning of Arabidopsis shoot apical meristems

Han

et al. 2020

Nat Commun

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“…In support of the latter hypothesis, we demonstrate that WUS acts via de-acetylation of histones and that interfering with HDAC activity triggers auxin responses in stem cells. However, there is evidence supporting both scenarios 23,25,27,28 Importantly, in addition to its effects on auxin signaling, WUS enhances cytokinin responses via the repression of negative feedback regulators 24 . This interaction can be overridden by expression of constitutively active versions of these negative feedback components 24 , and similarly we find here that dominant negative auxin regulators lead to SAM arrest.…”

Section: Discussionmentioning

confidence: 99%

WUSCHEL acts as a rheostat on the auxin pathway to maintain apical stem cells inArabidopsis

Miotk

Šutiković

et al. 2018

Preprint

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To maintain the balance between long-term stem cell self-renewal and differentiation, dynamic signals need to be translated into spatially precise and temporally stable gene expression states. In the apical plant stem cell system, local accumulation of the small, highly mobile phytohormone auxin triggers differentiation while at the same time, pluripotent stem cells are maintained throughout the entire life-cycle. We find that stem cells are resistant to auxin mediated differentiation, but require low levels of signaling for their maintenance. We demonstrate that the WUSCHEL transcription factor confers this behavior by rheostatically controlling the auxin signaling and response pathway.Finally, we show that WUSCHEL acts via regulation of histone acetylation at target loci, including those with functions in the auxin pathway. Our results reveal an important mechanism that allows cells to differentially translate a potent and highly dynamic developmental signal into stable cell behavior with high spatial precision and temporal robustness.

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“…Confinement of CLV3 expression to the region above the WUS domain is dependent on HAM1, a transcription factor in the rib zone. Interaction with HAM1 prevents WUS from activating CLV3 transcription, which restricts CLV3 expression to the apical region of the SAM (Zhou et al, 2018). It remains, however, unclear why WUS and CLV3 are expressed only around the central vertical axis of the SAM.…”

Section: Introductionmentioning

confidence: 99%

“…It remains, however, unclear why WUS and CLV3 are expressed only around the central vertical axis of the SAM. Previous mathematical models have used implicit or explicit assumptions to define the lateral boundary that confines the expression of WUS and CLV3 (Gruel et al, 2018;Zhou et al, 2018), but little is known about the actual existence of such a lateral signal. Here we present data showing that ERECTA family signaling restricts WUS and CLV3 expression laterally, confining them to the center of the meristem thereby providing a key mechanism for SAM maintenance.…”

Section: Introductionmentioning

confidence: 99%

ERECTA family signaling constrainsCLAVATA3andWUSCHELto the center of the shoot apical meristem

Zhang

DeGennaro

Lin

et al. 2020

Preprint

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2 Summary statementERf signaling restricts the width of the shoot apical meristem, a structure which generates aboveground plant organs, by inhibiting expression of two principal regulators, CLV3 and WUS, at its periphery. Abstract: The shoot apical meristem (SAM) is a reservoir of stem cells that gives rise to all post-embryonic aboveground plant organs. The size of the SAM remains stable over time due to a precise balance of stem cell replenishment versus cell incorporation into organ primordia. The WUSCHEL (WUS)/CLAVATA (CLV) negative feedback loop is central to SAM size regulation. Its correct function depends on accurate spatial expression of WUS and CLV3. A signaling pathway, consisting of ERECTA family (ERf) receptors and EPIDERMAL PATTERNING FACTOR LIKE (EPFL) ligands, restricts SAM width and promotes leaf initiation. While ERf receptors are expressed throughout the SAM, EPFL ligands are expressed in its periphery. Our genetic analysis demonstrated that ERfs and CLV3 synergistically regulate the size of the SAM, and wus is epistatic to erfs. Furthermore, activation of ERf signaling withexogenous EPFLs resulted in a rapid decrease of CLV3 and WUS expression. ERf-EPFL signaling inhibits expression of WUS and CLV3 in the periphery of the SAM, confining them to the center. These findings establish the molecular mechanism for stem cell positioning along the radial axis.

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HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers

Cited by 124 publications

References 34 publications

A signal cascade originated from epidermis defines apical-basal patterning of Arabidopsis shoot apical meristems

A signal cascade originated from epidermis defines apical-basal patterning of Arabidopsis shoot apical meristems

WUSCHEL acts as a rheostat on the auxin pathway to maintain apical stem cells inArabidopsis

ERECTA family signaling constrainsCLAVATA3andWUSCHELto the center of the shoot apical meristem

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