How was apical growth regulated in the ancestral land plant? Insights from the development of non-seed plants

Fouracre, Jim P.; Harrison, Conrad

doi:10.1093/plphys/kiac313

Cited by 28 publications

(14 citation statements)

References 169 publications

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“…Bryophytes, ferns and lycophytes rely on free-living gametophytes for reproduction (Fouracre and Harrison, 2022). Unlike mosses and liverworts whose dominant generation is the gametophyte (Frangedakis et al, 2023), the dominant generation in ferns is the sporophyte.…”

Section: Discussionmentioning

confidence: 99%

Efficient Gene Editing and Overexpression of Gametophyte Transformation in a Model Fern

Jiang,

Deng,

Babla

et al. 2024

Preprint

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The clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-related nuclease (Cas) system allows precise and easy editing of genes in many plant species. However, this system has not yet been applied to any fern species due to the complex characteristics of fern genomes, genetics and physiology. Here, we established, for the first time, a protocol for gametophyte-based screening single-guide RNAs (sgRNAs) with high efficiency for CRISPR/Cas-mediated gene editing in a model fern species, Ceratopteris richardii. We utilized the C. richardii Actin promoter to drive sgRNA expression and enhanced CaMV 35S promoter to drive the expression of Streptococcus pyogenes Cas9 in this CRISPR-mediated editing system, which was employed to successfully edit a few genes (e.g., nucleotidase/phosphatase 1, CrSAL1; Cryptochrome 4, CRY4) and CrPDS, encoding a phytoene desaturase protein that resulted in an albino phenotype in C. richardii. Knockout of CrSAL1 resulted in significantly reduced stomatal conductance (gs), leaf transpiration rate (E), stomatal/pore length, and abscisic acid (ABA)-induced reactive oxygen species (ROS) accumulation in guard cells. Moreover, CrSAL1 overexpressing plants showed significantly increased net photosynthetic rate (A), gs, E and intrinsic water use efficiency (iWUE) as well as most of the stomatal traits and ROS production in guard cells compared to those in the wild-type (WT) plants. Taken together, the optimized CRISPR/Cas9 system provides a useful tool for functional genomics in a model fern species, allowing the exploration of fern gene functions for evolutionary biology, herbal medicine discovery and agricultural applications.

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Section: Discussionmentioning

confidence: 99%

Efficient Gene Editing and Overexpression of Gametophyte Transformation in a Model Fern

Jiang,

Deng,

Babla

et al. 2024

Preprint

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“…ERfs do this independently of WUS , since in the central zone of the er erl1 erl2 mutant the CLV3 cellular expression increases without an increase of WUS expression, and knockout of ERf signaling in the wus background promotes CLV3 expression (Kimura et al, 2018). In meristematic cells of bryophytes, CLV signaling regulates auxin and cytokinin signaling, and it does it independently of WUS homeobox-containing ( WOX ) genes (Fouracre and Harrison, 2022). CLV3 signaling might have additional unknown targets in angiosperms, and suppression of CLV3 by ERfs might be related to these other functions.…”

Section: Discussionmentioning

confidence: 99%

An updated model of shoot apical meristem regulation by ERECTA family and CLAVATA3 signaling pathways

Uzair,

Urquidi Camacho,

Liu

et al. 2023

Preprint

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The shoot apical meristem (SAM) gives rise to above-ground organs. The size of the SAM is relatively constant due to the balance of stem cell replenishment versus cell recruitment into developing organs. In angiosperms, the transcription factor WUSCHEL (WUS) promotes stem cell identity in the central zone of the SAM. WUS forms a negative feedback loop with a signaling pathway activated by CLAVATA3 (CLV3). In the periphery of the SAM, the ERECTA family (ERf) receptors promote cell differentiation and constrain the expression ofWUSandCLV3. Here, we show that four ligands of ERfs redundantly inhibitCLV3andWUSexpression. Transcriptome analysis confirmed thatWUSandCLV3are the main targets of ERf signaling and uncovered several new ones. Analysis of promoter reporters indicated that in the vegetative meristem, theWUSexpression domain mostly overlapped with theCLV3domain and did not shift along the apical-basal axis inclv3. A 3D mathematical model reproduced the experimentally observedCLV3andWUSexpression patterns with fewer assumptions than earlier models. Based on these findings, we propose that CLV3 regulates cellular levels ofWUSexpression through autocrine signaling, while ERfs regulateWUSspatial expression, preventing its encroachment into the peripheral zone.One Sentence SummaryThrough autocrine signaling, CLV3 regulates the level ofWUSexpression in the vegetative SAM but not its location, while ERfs regulate theWUSspatial pattern, preventing its expansion into the peripheral zone.

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“…Each row consists of basally arranged meristematic cells that continuously differentiate into the major tissue types towards the apex of the sporophyte. Very little is known about the molecular mechanisms governing the development of this meristem and its evolutionary homology to the multicellular meristems of land plants is highly debated ( Ligrone et al., 2012a ; Ligrone et al., 2012b ; Harrison and Morris, 2018 ; Fouracre and Harrison, 2022 ). Nevertheless, the continuous differentiation gradient present along the longitudinal axis of the sporophyte provides an excellent model to understand conserved features of cell fate determination across bryophytes and vascular plants, and potentially the origin of multicellular meristems in vascular plants.…”

Section: The Unique Biology Of Hornwortsmentioning

confidence: 99%

What can hornworts teach us?

et al. 2023

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The hornworts are a small group of land plants, consisting of only 11 families and approximately 220 species. Despite their small size as a group, their phylogenetic position and unique biology are of great importance. Hornworts, together with mosses and liverworts, form the monophyletic group of bryophytes that is sister to all other land plants (Tracheophytes). It is only recently that hornworts became amenable to experimental investigation with the establishment of Anthoceros agrestis as a model system. In this perspective, we summarize the recent advances in the development of A. agrestis as an experimental system and compare it with other plant model systems. We also discuss how A. agrestis can help to further research in comparative developmental studies across land plants and to solve key questions of plant biology associated with the colonization of the terrestrial environment. Finally, we explore the significance of A. agrestis in crop improvement and synthetic biology applications in general.

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How was apical growth regulated in the ancestral land plant? Insights from the development of non-seed plants

Cited by 28 publications

References 169 publications

Efficient Gene Editing and Overexpression of Gametophyte Transformation in a Model Fern

Efficient Gene Editing and Overexpression of Gametophyte Transformation in a Model Fern

An updated model of shoot apical meristem regulation by ERECTA family and CLAVATA3 signaling pathways

What can hornworts teach us?

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