Elsevier

Current Opinion in Plant Biology

Volume 58, December 2020, Pages 17-24
Current Opinion in Plant Biology

Lonely at the top? Regulation of shoot apical meristem activity by intrinsic and extrinsic factors

https://doi.org/10.1016/j.pbi.2020.08.008Get rights and content

All the above-ground organs of a plant are derived from stem cells that reside in shoot apical meristems (SAM). Over the past 25 years, the genetic pathways that control the proliferation of stem cells within the SAM, and the differentiation of their progenitors into lateral organs, have been described in great detail. However, longstanding questions regarding the importance of communication between cells within the SAM and lateral organs have, until recently, remained unanswered. In this review, we describe recent investigations into the extent, nature and significance of signaling both to and from the SAM.

Introduction

The growth and architecture of a plant shoot depend on the activity of shoot apical meristems (SAMs). These structures are stably maintained by the precisely controlled balance between cell proliferation and differentiation, but are also capable of responding to endogenous and environmental cues that influence their growth and the types of organs they produce. The degree to which the SAM regulates shoot development autonomously, or acts in response to extrinsic factors that originate outside the SAM, is a classic question in plant biology. Half a century ago, Ian Sussex [1] asked: ‘are … meristems to be considered as organizer regions whose functional changes represent changes initiated within the meristem itself, or are they simply plastic regions in which new cells are molded into organs and tissues in response to stimuli proceeding from other sources?’ At the time, data from microsurgical, shoot culture, and hormone treatment studies suggested that the SAM was largely autonomous of neighboring tissues and organs. However, with the benefit of modern molecular tools, it has become apparent that apical meristems typically function as signaling integrators, coordinating cues from elsewhere in the plant and from the environment.

The structure and activity of the SAM, and the regulatory networks that determine these features, have been reviewed extensively recently [2,3]. SAMs possess several distinct functional domains (Figure 1). Stem cells — which divide to produce additional stem cells as well as cells that will differentiate — reside within the central zone (CZ). Cells derived from the CZ are displaced laterally to the peripheral zone (PZ), where they differentiate into lateral organs, or basally to the rib zone (RZ), where they differentiate into cells of the stem. Stem cell proliferation within the SAM is maintained by the activity of members of two distinct families of homeobox gene: WUSCHEL-LIKE (WOX) and KNOTTED-LIKE (KNOX). In Arabidopsis, WUSCHEL (WUS) is expressed in the ‘Organizing Center’ of the CZ (Figure 1), where it promotes the division of stem cells. The expression domain of WUS is restricted by the activity of the signaling peptide CLAVATA3 (CLV3), which regulates WUS in a negative feedback loop. Therefore loss-of CLV3 function leads to an expansion of the SAM, whereas loss-of WUS function leads to meristem termination. The Arabidopsis KNOX gene SHOOT MERISTEMLESS (STM) is expressed more broadly in the SAM, and acts to maintain stem cells in an undifferentiated state. Both WUS and STM are necessary for meristem maintenance throughout the ontogeny of individual meristems, and within different developmental contexts, that is, SAMs in the vegetative and reproductive phases of a plant life cycle. In this review, we detail how core developmental processes in the SAM are influenced by extrinsic genetic and metabolic factors, describe examples of environmental signals that are perceived both within and without the SAM, and provide an update on a long-standing hypothesis regarding extrinsic signaling by the SAM on lateral organs.

Section snippets

Regulation of developmental transitions by extrinsic factors

The best described example of an extrinsically regulated change in the activity of the SAM is floral induction (Figure 2a). It has been known for many years that inductive photoperiods trigger production of a mobile ‘florigen’ in leaves, which moves to the SAM to initiate flowering [4]. This signal is now known to be a small protein encoded by the FLOWERING LOCUS T (FT) gene. FT moves from leaves to the SAM via the phloem [5, 6, 7, 8], where it interacts with the locally expressed bZIP

Short-range signaling

As described in the introduction, the SAM is initiated and maintained by transcription factors (WUS and STM) that are expressed exclusively within the SAM. The distribution and activity of these transcription factors are regulated by molecules that are produced locally within the SAM, and by molecules produced by surrounding organs and tissues.

Several of these molecules act to repress the growth of the SAM. For example, although a basal level of auxin signaling is required for the maintenance

Intrinsic and extrinsic environmental regulation of SAM activity

In nature, plants modify their growth and development to adapt to varying environmental conditions. Although many of these responses involve changes in the activity of the SAM (e.g. the timing of developmental transitions, the rate of leaf initiation, branching patterns), it is usually unclear if the environmental stimulus is perceived directly by the SAM, or perceived elsewhere in the plant and transmitted to the SAM. For example, cold-induced repression of the floral suppressor FLC occurs in

Extrinsic regulation by the SAM?

A classic hypothesis in plant biology is that the SAM non-cell autonomously regulates dorsoventral patterning in leaves [76]. Taking into account microsurgical experiments in potato and tomato, it has been proposed that a SAM-derived signal is required to correctly induce leaf dorsoventrality [76,77]. However, evidence from laser-ablation of cells in the SAM has recently led to an alternative interpretation of these microsurgical experiments [78••]. Caggiano et al. demonstrated that wounding

Conclusion and outlook

Although the function of the SAM depends on integrating extrinsic signals, the core regulatory networks that coordinate stem cell proliferation appear to operate with minimal external input. The relative independence of these networks is demonstrated by the limited range of signals to which they are susceptible (Table 1). Plant hormones, microRNAs, sugars, and small proteins are all able to extrinsically regulate SAM activity, whereas there is little support for extrinsic regulation by larger

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

CRediT authorship contribution statement

Jim P Fouracre: Writing - original draft, Writing - review & editing. Richard Scott Poethig: Writing - review & editing.

Acknowledgements

We apologize to authors’ who’s works were unable to be included due to size constraints and thank members of the Poethig lab for useful discussions. Work in the Poethig lab on developmental transitions is funded by National Institutes of Health grant R01-GM51893 to R.S.P.

References (95)

  • I.M. Sussex

    The permanence of meristems: developmental organizers or reactors to exogenous stimuli?

    Meristems and Differentiation

    (1964)
  • M. Kitagawa et al.

    Control of meristem size

    Annu Rev Plant Biol

    (2019)
  • J.A.D. Zeevaart

    Physiology of flower formation

    Annu Rev Plant Physiol

    (1976)
  • L. Corbesier et al.

    FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis

    Science

    (2007)
  • S. Tamaki et al.

    Hd3a protein is a mobile flowering signal in rice

    Science

    (2007)
  • M. Abe et al.

    FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex

    Science

    (2005)
  • P.A. Wigge et al.

    Integration of spatial and temporal information during floral induction in Arabidopsis

    Science

    (2005)
  • S. Collani et al.

    FT modulates genome-wide DNA-binding of the bZIP transcription factor FD

    Plant Physiol

    (2019)
  • N. Kawamoto et al.

    Calcium-dependent protein kinases responsible for the phosphorylation of a bZIP transcription factor FD crucial for the florigen complex formation

    Sci Rep

    (2015)
  • S. Eriksson et al.

    GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation

    Plant Cell

    (2006)
  • R.W. King et al.

    Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex

    Plant Physiol

    (2001)
  • Y. Kanno et al.

    AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes

    Nat Commun

    (2016)
  • T. Regnault et al.

    The gibberellin precursor GA12 acts as a long-distance growth signal in Arabidopsis

    Nat Plants

    (2015)
  • F. Andrés et al.

    SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition

    Proc Natl Acad Sci U S A

    (2014)
  • C.W. Wardlaw

    The morphogenetic rôle of apical meristems: fundamental aspects (illustrated by means of the shoot apical meristem)

  • L. Yang et al.

    Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156

    Development

    (2011)
  • L. Yang et al.

    Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C

    eLife

    (2013)
  • S. Yu et al.

    Sugar is an endogenous cue for juvenile-to-adult phase transition in plants

    eLife

    (2013)
  • J.W. Wang et al.

    Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana

    Plant Cell

    (2008)
  • J.P. Fouracre et al.

    Role for the shoot apical meristem in the specification of juvenile leaf identity in Arabidopsis

    Proc Natl Acad Sci U S A

    (2019)
  • H. Han et al.

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

    Nat Commun

    (2020)
  • D.S. Skopelitis et al.

    Gating of miRNA movement at defined cell-cell interfaces governs their impact as positional signals

    Nat Commun

    (2018)
  • B. Shi et al.

    Feedback from lateral organs controls shoot apical meristem growth by modulating auxin transport

    Dev Cell

    (2018)
  • A. Goldshmidt et al.

    Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of Arabidopsis shoot apical meristems

    Plant Cell

    (2008)
  • B.I. Je et al.

    Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits

    Nat Genet

    (2016)
  • S. Knauer et al.

    A high-resolution gene expression atlas links dedicated meristem genes to key architectural traits

    Genome Res

    (2019)
  • M.J. Prigge et al.

    Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development

    Plant Cell

    (2005)
  • Q. Liu et al.

    The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis

    Plant J

    (2009)
  • S. Miyashima et al.

    A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function

    Plant Cell Physiol

    (2013)
  • K. Lynn et al.

    The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene

    Development

    (1999)
  • M.R. Tucker et al.

    Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo

    Development

    (2008)
  • H. Zhu et al.

    Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development

    Cell

    (2011)
  • Y. Yu et al.

    ARGONAUTE10 promotes the degradation of miR165/6 through the SDN1 and SDN2 exonucleases in Arabidopsis

    PLoS Biol

    (2017)
  • S. Naramoto et al.

    A conserved regulatory mechanism mediates the convergent evolution of plant shoot lateral organs

    PLoS Biol

    (2019)
  • C.A. MacAlister et al.

    Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene

    Nat Genet

    (2012)
  • S. Takeda et al.

    CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells

    Plant J

    (2011)
  • A. Yoshida et al.

    TAWAWA1, a regulator of rice inflorescence architecture, functions through the suppression of meristem phase transition

    Proc Natl Acad Sci U S A

    (2013)
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