Integration of Core Mechanisms Underlying Plant Aerial Architecture

Heisler, Marcus G.

doi:10.3389/fpls.2021.786338

Cited by 8 publications

(5 citation statements)

References 120 publications

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“…(2017) proposed that HD-ZIP III and KAN both inhibit auxin, leaving a maximum of auxin activity in the HD-ZIP III – KAN interface zone. This is consistent with the role of PIN1-auxin PAT in regulating primordia development within the initiation zone ( Reinhardt et al., 2003 ; Hakman et al., 2009 ), and auxin’s role in morphogenetic outgrowth ( Heisler, 2021 ).…”

Section: Discussionsupporting

confidence: 86%

Size regulation of the lateral organ initiation zone and its role in determining cotyledon number in conifers

2023

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IntroductionUnlike monocots and dicots, many conifers, particularly Pinaceae, form three or more cotyledons. These are arranged in a whorl, or ring, at a particular distance from the embryo tip, with cotyledons evenly spaced within the ring. The number of cotyledons, nc, varies substantially within species, both in clonal cultures and in seed embryos. nc variability reflects embryo size variability, with larger diameter embryos having higher nc. Correcting for growth during embryo development, we extract values for the whorl radius at each nc. This radius, corresponding to the spatial pattern of cotyledon differentiation factors, varies over three-fold for the naturally observed range of nc. The current work focuses on factors in the patterning mechanism that could produce such a broad variability in whorl radius. Molecularly, work in Arabidopsis has shown that the initiation zone for leaf primordia occurs at a minimum between inhibitor zones of HD-ZIP III at the shoot apical meristem (SAM) tip and KANADI (KAN) encircling this farther from the tip. PIN1-auxin dynamics within this uninhibited ring form auxin maxima, specifying primordia initiation sites. A similar mechanism is indicated in conifer embryos by effects on cotyledon formation with overexpression of HD-ZIP III inhibitors and by interference with PIN1-auxin patterning.MethodsWe develop a mathematical model for HD-ZIP III/KAN spatial localization and use this to characterize the molecular regulation that could generate (a) the three-fold whorl radius variation (and associated nc variability) observed in conifer cotyledon development, and (b) the HD-ZIP III and KAN shifts induced experimentally in conifer embryos and in Arabidopsis.ResultsThis quantitative framework indicates the sensitivity of mechanism components for positioning lateral organs closer to or farther from the tip. Positional shifting is most readily driven by changes to the extent of upstream (meristematic) patterning and changes in HD-ZIP III/KAN mutual inhibition, and less efficiently driven by changes in upstream dosage or the activation of HD-ZIP III. Sharper expression boundaries can also be more resistant to shifting than shallower expression boundaries.DiscussionThe strong variability seen in conifer nc (commonly from 2 to 10) may reflect a freer variation in regulatory interactions, whereas monocot (nc = 1) and dicot (nc = 2) development may require tighter control of such variation. These results provide direction for future quantitative experiments on the positional control of lateral organ initiation, and consequently on plant phyllotaxy and architecture.

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Section: Discussionsupporting

confidence: 86%

Size regulation of the lateral organ initiation zone and its role in determining cotyledon number in conifers

2023

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“…Members of the HD-ZIP III family were shown to control SAM activity, radial patterning, and organogenesis to various extents [ 40 , 48 , 49 , 116 , 117 , 118 ]. SAM organogenesis relies on auxin accumulation in the peripheral zone (PZ) to promote organ initiation and subsequent primordium emergence [ 119 , 120 ]. PIN1-mediated transport promotes IAA accumulation at the PZ, causing the activation of ARF-dependent and -independent signaling pathways [ 32 , 121 , 122 , 123 ].…”

Section: Sam Maintenance and Organogenesismentioning

confidence: 99%

The Ins and Outs of Homeodomain-Leucine Zipper/Hormone Networks in the Regulation of Plant Development

Sessa,

Carabelli,

Sassi

2024

IJMS

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The generation of complex plant architectures depends on the interactions among different molecular regulatory networks that control the growth of cells within tissues, ultimately shaping the final morphological features of each structure. The regulatory networks underlying tissue growth and overall plant shapes are composed of intricate webs of transcriptional regulators which synergize or compete to regulate the expression of downstream targets. Transcriptional regulation is intimately linked to phytohormone networks as transcription factors (TFs) might act as effectors or regulators of hormone signaling pathways, further enhancing the capacity and flexibility of molecular networks in shaping plant architectures. Here, we focus on homeodomain-leucine zipper (HD-ZIP) proteins, a class of plant-specific transcriptional regulators, and review their molecular connections with hormonal networks in different developmental contexts. We discuss how HD-ZIP proteins emerge as key regulators of hormone action in plants and further highlight the fundamental role that HD-ZIP/hormone networks play in the control of the body plan and plant growth.

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“…Given that epidermal auxin convergence points were proposed as the trigger for auxin movement into internal cells (Scarpella et al ., 2006), but recent experiments revealed that they are neither necessary or sufficient for midvein formation in Arabidopsis (Govindaraju et al ., 2020; Lavania et al ., 2021), unknown components of auxin flux mechanisms obviously exist. In this context, both experimental and modelling approaches have suggested that mechanical stresses mediated by microtubule and cellulose microfibril dynamics play a role in both UTG and WTF movement of auxin, and it is becoming increasingly clear that the significance of auxin‐driven reorientation of PIN1 proteins during leaf primordium and midvein formation needs to be reevaluated in a more complex framework than previously considered (recently discussed and reviewed in Heisler, 2021; ten Tusscher, 2021; Vernoux et al ., 2021).…”

Section: Ontogeny Of Leaf Veinsmentioning

confidence: 99%

Developmental regulation of leaf venation patterns: monocot versus eudicots and the role of auxin

2022

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Summary Organisation and patterning of the vascular network in land plants varies in different taxonomic, developmental and environmental contexts. In leaves, the degree of vascular strand connectivity influences both light and CO2 harvesting capabilities as well as hydraulic capacity. As such, developmental mechanisms that regulate leaf venation patterning have a direct impact on physiological performance. Development of the leaf venation network requires the specification of procambial cells within the ground meristem of the primordium and subsequent proliferation and differentiation of the procambial lineage to form vascular strands. An understanding of how diverse venation patterns are manifest therefore requires mechanistic insight into how procambium is dynamically specified in a growing leaf. A role for auxin in this process was identified many years ago, but questions remain. In this review we first provide an overview of the diverse venation patterns that exist in land plants, providing an evolutionary perspective. We then focus on the developmental regulation of leaf venation patterns in angiosperms, comparing patterning in eudicots and monocots, and the role of auxin in each case. Although common themes emerge, we conclude that the developmental mechanisms elucidated in eudicots are unlikely to fully explain how parallel venation patterns in monocot leaves are elaborated.

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Integration of Core Mechanisms Underlying Plant Aerial Architecture

Cited by 8 publications

References 120 publications

Size regulation of the lateral organ initiation zone and its role in determining cotyledon number in conifers

Size regulation of the lateral organ initiation zone and its role in determining cotyledon number in conifers

The Ins and Outs of Homeodomain-Leucine Zipper/Hormone Networks in the Regulation of Plant Development

Developmental regulation of leaf venation patterns: monocot versus eudicots and the role of auxin

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