Land plants develop highly diversified shoot architectures, all of which are derived from the pluripotent stem cells in shoot apical meristems (SAMs). As sustainable resources for continuous organ formation in the aboveground tissues, SAMs play an important role in determining plant yield and biomass production. In this review, we summarize recent advances in understanding one group of key regulators – the HAIRY MERISTEM (HAM) family GRAS domain proteins – in shoot meristems. We highlight the functions of HAM family members in dictating shoot stem cell initiation and proliferation, the signaling cascade that shapes HAM expression domains in shoot meristems, and the conservation and diversification of HAM family members in land plants. We also discuss future directions that potentially lead to a more comprehensive view of the HAM gene family and stem cell homeostasis in land plants. 
                        more » 
                        « less   
                    
                            
                            Conservation and diversification of HAIRY MERISTEM gene family in land plants
                        
                    
    
            SUMMARY The shoot apical meristems (SAMs) of land plants are crucial for plant growth and organ formation. In several angiosperms, theHAIRY MERISTEM(HAM) genes function as key regulators that control meristem development and stem cell homeostasis. To date, the origin and evolutionary history of the HAM family in land plants remains unclear. Potentially shared and divergent functions of HAM family members from angiosperms and non‐angiosperms are also not known. In constructing a comprehensive phylogeny of the HAM family, we show that HAM proteins are widely present in land plants and that HAM proteins originated prior to the divergence of bryophytes. The HAM family was duplicated in a common ancestor of angiosperms, leading to two distinct groups: type I and type II. Type‐II HAM members are widely present in angiosperms, whereas type‐I HAM members were independently lost in different orders of monocots. Furthermore, HAM members from angiosperms and non‐angiosperms (including bryophytes, lycophytes, ferns and gymnosperms) are able to replace the role of the type‐IIHAMgenes in Arabidopsis, maintaining established SAMs and promoting the initiation of new stem cell niches. Our results uncover the conserved functions of HAM family members and reveal the conserved regulatory mechanisms underlying HAM expression patterning in meristems, providing insight into the evolution of key stem cell regulators in land plants. 
        more » 
        « less   
        
    
                            - Award ID(s):
- 1931114
- PAR ID:
- 10452962
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 106
- Issue:
- 2
- ISSN:
- 0960-7412
- Page Range / eLocation ID:
- p. 366-378
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
- 
            
- 
            ABSTRACT A fascinating feature of land plants is their ability to continually initiate new tissues and organs throughout their lifespan, driven by a pool of pluripotent stem cells located in meristems. In seed plants, various types of meristems are initiated and maintained during the sporophyte generation, while their gametophytes lack meristems and rely on sporophyte tissues for growth. In contrast, seed‐free vascular plants, such as ferns, develop meristems during both the sporophyte and gametophyte generations, allowing for the independent growth of both generations. Recent findings have highlighted both conserved and lineage‐specific roles of the HAIRY MERISTEM (HAM) family of GRAS‐domain transcriptional regulators in various meristems throughout the land plant lifecycle. Here, we review and discuss howHAMgenes maintain meristem indeterminacy in both sporophytes and gametophytes, with a focus on studies performed in two model species: the flowering plantArabidopsis thalianaand the fernCeratopteris richardii. Additionally, we summarize the crucial and tightly regulated functions of the microRNA171 (miR171)‐HAM regulatory modules, which define HAM spatial patterns and activities during meristem development across various meristem identities in land plants.more » « less
- 
            MicroRNA171 (miR171), a group of 21-nucleotide single-strand small RNAs, is one ancient and conserved microRNA family in land plants. This review focuses on the recent progress in understanding the role of miR171 in plant stem cell homeostasis and developmental patterning, and the regulation of miR171 by developmental cues and environmental signals. Specifically, miR171 regulates shoot meristem activity and phase transition through repressing the HAIRYMERISTEM (HAM) family genes. In the model species Arabidopsis, miR171 serves as a short-range mobile signal, which initiates in the epidermal layer of shoot meristems and moves downwards within a limited distance, to pattern the apical-basal polarity of gene expression and drive stem cell dynamics. miR171 levels are regulated by light and various abiotic stresses, suggesting miR171 may serve as a linkage between environmental factors and cell fate decisions. Furthermore, miR171 family members also demonstrate both conserved and lineage-specific functions in land plants, which are summarized and discussed here.more » « less
- 
            Abstract The precise regulation of stem cells in the shoot apical meristems (SAMs) involves the function of the homeodomain transcription factor (TF)‐WUSCHEL (WUS). WUS has been shown to move from the site of production‐the rib‐meristem (RM), into overlaying cells of the central zone (CZ), where it specifies stem cells and also regulates the transcription ofCLAVATA3 (CLV3). The secreted signalling peptide CLV3 activates a receptor kinase signalling that restrictsWUStranscription and also regulates the nuclear gradient of WUS by offsetting nuclear export. WUS has been shown to regulate bothCLV3levels and spatial activation, restricting its expression to a few cells in the CZ. The HAIRY MERISTEM (HAM), a GRASS‐domain class of TFs expressed in the RM, has been shown to physically interact with WUS and regulateCLV3expression. However, the mechanisms by which this interaction regulatesCLV3expression non‐cell autonomously remain unclear. Here, we show that HAM function is required for regulating the WUS protein stability, and theCLV3expression responds to altered WUS protein levels inhammutants. Thus, HAM proteins non‐cell autonomously regulatesCLV3expression.more » « less
- 
            The life cycle of land plants is characterized by alternating generations of sexual gametophytes and asexual sporophytes. Unlike seed plants, seed-free vascular plants, including ferns, initiate and maintain pluripotent meristems during their gametophyte phase to sustain body expansion and drive the formation of sexual organs for reproduction. This review summarizes meristem development among various fern species during the gametophyte phase, focusing on the cellular basis of meristem initiation, proliferation, and termination. We review the different types of gametophytic meristems in ferns, including apical cell (AC)-based meristems, multicellular apical meristems, and multicellular marginal meristems. We highlight both conserved and lineage-specific patterns of cell division, which are closely associated with these meristem identities and play crucial roles in shaping gametophytic morphology. Additionally, we highlight recent progress in understanding the dynamics of cell division and growth that drive meristem development, through studies that integrate confocal live imaging and computational quantitative analysis. Furthermore, we discuss the influence of environmental and genetic factors on cell division activity in fern gametophytes, including conserved transcriptional regulators that sustain meristem indeterminacy and proliferation in the model fern Ceratopteris richardii.more » « less
 An official website of the United States government
An official website of the United States government 
				
			 
					 
					
