Lonely at the top? Regulation of shoot apical meristem activity by intrinsic and extrinsic factors
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)
- et al.
Transcriptional circuits in control of shoot stem cell homeostasis
Curr Opin Plant Biol
(2020) - et al.
FT protein acts as a long-range signal in Arabidopsis
Curr Biol
(2007) - et al.
Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis
Curr Biol
(2007) Vegetative phase change and shoot maturation in plants
Curr Top Dev Biol
(2013)- et al.
A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem
Dev Cell
(2013) - et al.
WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis
Nat Commun
(2019) - et al.
Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots
Nature
(2001) - et al.
Beyond the divide: boundaries for patterning and stem cell regulation in plants
Front Plant Sci
(2015) - et al.
Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes
Proc Natl Acad Sci U S A
(2017) - et al.
Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis
Nat Commun
(2017)