From Genes to Shape and Function: Leaf Morphogenesis at Play

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Development and Morphogenesis".

Deadline for manuscript submissions: closed (30 August 2019) | Viewed by 69113

Special Issue Editor


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Guest Editor
Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, RD10, CEDEX, 78026 Versailles, France
Interests: leaf; boundary domain; growth; microRNA; transcription factors; hormones

Special Issue Information

Dear Colleagues,

Leaves are not only the main photosynthetic organs of plants and, as such, critical to plant growth and biomass production, but also provide wonderful models to study how complex biological shapes arise from simple structures, what are the evolutionary mechanisms leading to shape variation between species, and how developmental or environmental cues act to generate shape plasticity within an organism. For instance, studies on the polarization of the leaf into abaxial or adaxial domains have provided insights into the mechanisms behind patterning into different domains. Studies on leaf growth enlighten how hormones, transcription factors and small RNAs interact to regulate cell proliferation and expansion, and how these processes are integrated at the whole organ level to regulate leaf shape and size. Beside such studies that enrich our understanding of the molecular and cellular mechanisms that contribute to organ shape elaboration, other comparative analyses between species with contrasted shapes have examplified how the apparition of a new actor, or rewiring the interactions between existing ones, can modify the regulatory network leading to shape innovations during evolution. An emerging field is to build on the knowledge of the mechanisms at play during morphogenesis to understand how they may be modified by environmental signals, such as light quantity or quality or temperature, to allow leaf plasticity. Finally, a standing question that is both of fundamental and applied interest, is the adaptive value of leaf shape in relation with its photosynthetic activity.

This Special Issue welcomes all types of papers (research papers, methods, reviews) addressing either the molecular, genetic or cellular mechanisms acting during leaf morphogenesis, their flexibility during evolution or under different environmental conditions, or the functional significance of different leaf morphologies.

Dr. Patrick Laufs
Guest Editor

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Keywords

  • leaf
  • morphogenesis
  • patterning
  • growth
  • microRNA
  • transcription factors
  • hormones
  • plasticity
  • shape evolution
  • organ shape/function relationship

Published Papers (9 papers)

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Research

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28 pages, 6690 KiB  
Article
Transcription Factor Networks in Leaves of Cichorium endivia: New Insights into the Relationship between Photosynthesis and Leaf Development
by Giulio Testone, Elena Baldoni, Maria Adelaide Iannelli, Chiara Nicolodi, Elisabetta Di Giacomo, Fabrizio Pietrini, Giovanni Mele, Donato Giannino and Giovanna Frugis
Plants 2019, 8(12), 531; https://doi.org/10.3390/plants8120531 - 21 Nov 2019
Cited by 9 | Viewed by 4027
Abstract
Cichorium endivia is a leafy crop closely related to Lactuca sativa that comprises two major botanical varieties characterized by a high degree of intraspecific morphological variation: var. latifolium with broad leaves (escarole) and var. crispum with narrow crisp curly leaves (endive). To investigate [...] Read more.
Cichorium endivia is a leafy crop closely related to Lactuca sativa that comprises two major botanical varieties characterized by a high degree of intraspecific morphological variation: var. latifolium with broad leaves (escarole) and var. crispum with narrow crisp curly leaves (endive). To investigate the relationship between leaf morphology and photosynthetic activity, escaroles and endives were used as a crop model due to the striking morphological diversity of their leaves. We constructed a leaf database for transcription factors (TFs) and photosynthesis-related genes from a refined C. endivia transcriptome and used RNA-seq transcriptomic data from leaves of four commercial endive and escarole cultivars to explore transcription factor regulatory networks. Cluster and gene co-expression network (GCN) analyses identified two main anticorrelated modules that control photosynthesis. Analysis of the GCN network topological properties identified known and novel hub genes controlling photosynthesis, and candidate developmental genes at the boundaries between shape and function. Differential expression analysis between broad and curly leaves suggested three novel TFs putatively involved in leaf shape diversity. Physiological analysis of the photosynthesis properties and gene expression studies on broad and curly leaves provided new insights into the relationship between leaf shape and function. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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17 pages, 2750 KiB  
Article
Leaf Production and Expansion: A Generalized Response to Drought Stresses from Cells to Whole Leaf Biomass—A Case Study in the Tomato Compound Leaf
by Garance Koch, Gaëlle Rolland, Myriam Dauzat, Alexis Bédiée, Valentina Baldazzi, Nadia Bertin, Yann Guédon and Christine Granier
Plants 2019, 8(10), 409; https://doi.org/10.3390/plants8100409 - 12 Oct 2019
Cited by 27 | Viewed by 4314
Abstract
It is clearly established that there is not a unique response to soil water deficit but that there are as many responses as soil water deficit characteristics: Drought intensity, drought duration, and drought position during plant cycle. For a same soil water deficit, [...] Read more.
It is clearly established that there is not a unique response to soil water deficit but that there are as many responses as soil water deficit characteristics: Drought intensity, drought duration, and drought position during plant cycle. For a same soil water deficit, responses can also differ on plant genotype within a same species. In spite of this variability, at least for leaf production and expansion processes, robust tendencies can be extracted from the literature when similar watering regimes are compared. Here, we present response curves and multi-scale dynamics analyses established on tomato plants exposed to different soil water deficit treatments. Results reinforce the trends already observed for other species: Reduction in plant leaf biomass under water stress was due to reduction in individual leaf biomass and areas whereas leaf production and specific leaf area were not affected. The dynamics of leaf expansion was modified both at the leaf and cell scales. Cell division and expansion were reduced by drought treatments as well as the endoreduplication process. Combining response curves analyses together with dynamic analyses of tomato compound leaf growth at different scales not only corroborate results on simple leaf responses to drought but also increases our knowledge on the cellular mechanisms behind leaf growth plasticity. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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11 pages, 2699 KiB  
Article
The Evolution of the KANADI Gene Family and Leaf Development in Lycophytes and Ferns
by Cecilia Zumajo-Cardona, Alejandra Vasco and Barbara A. Ambrose
Plants 2019, 8(9), 313; https://doi.org/10.3390/plants8090313 - 30 Aug 2019
Cited by 31 | Viewed by 6834
Abstract
Leaves constitute the main photosynthetic plant organ and even though their importance is not debated, the origin and development of leaves still is. The leaf developmental network has been elucidated for angiosperms, from genes controlling leaf initiation, to leaf polarity and shape. There [...] Read more.
Leaves constitute the main photosynthetic plant organ and even though their importance is not debated, the origin and development of leaves still is. The leaf developmental network has been elucidated for angiosperms, from genes controlling leaf initiation, to leaf polarity and shape. There are four KANADI (KAN) paralogs in Arabidopsis thaliana needed for organ polarity with KAN1 and KAN2 specifying abaxial leaf identity. Yet, studies of this gene lineage outside angiosperms are required to better understand the evolutionary patterns of leaf development and the role of KAN homologs. We studied the evolution of KAN genes across vascular plants and their expression by in situ hybridization in the fern, Equisetum hyemale and the lycophyte Selaginella moellendorffii. Our results show that the expression of KAN genes in leaves is similar between ferns and angiosperms. However, the expression patterns observed in the lycophyte S. moellendorffii are significantly different compared to all other vascular plants, suggesting that the KAN function in leaf polarity is likely only conserved across ferns, gymnosperms, and angiosperms. This study indicates that mechanisms for leaf development are different in lycophytes compared to other vascular plants. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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19 pages, 2448 KiB  
Article
Determinants of Shoot Biomass Production in Mulberry: Combined Selection with Leaf Morphological and Physiological Traits
by Xu Cao, Qiudi Shen, Chunqiong Shang, Honglei Yang, Li Liu and Jialing Cheng
Plants 2019, 8(5), 118; https://doi.org/10.3390/plants8050118 - 06 May 2019
Cited by 12 | Viewed by 4082
Abstract
Physiological and morphological traits have a considerable impact on the biomass production of fast-growing trees. To compare cultivar difference in shoot biomass and investigate its relationships with leaf functional traits in mulberry, agronomic traits and 20 physiological and morphological attributes of 3-year-old mulberry [...] Read more.
Physiological and morphological traits have a considerable impact on the biomass production of fast-growing trees. To compare cultivar difference in shoot biomass and investigate its relationships with leaf functional traits in mulberry, agronomic traits and 20 physiological and morphological attributes of 3-year-old mulberry trees from eight cultivars growing in a common garden were analyzed. The cultivars Xiang7920, Yu711, and Yunsang2 had higher shoot fresh biomass (SFB), which was closely associated with their rapid leaf expansion rate, large leaf area, and high stable carbon isotope composition (δ13C). Conversely, the cultivars 7307, Husang32, Wupu, Yunguo1, and Liaolu11 were less productive, and this was primarily the result of slower leaf expansion and smaller leaf size. Growth performance was negatively correlated with leaf δ13C and positively correlated with the total nitrogen concentration, indicating that a compromise exists in mulberry between water use efficiency (WUE) (low δ13C) and high nitrogen consumption for rapid growth. Several morphological traits, including the maximum leaf area (LAmax), leaf width and length, petiole width and length, leaf number per shoot, and final shoot height were correlated with SFB. The physiological traits that were also influential factors of shoot biomass were the leaf δ13C, the total nitrogen concentration, and the water content. Among the studied leaf traits, LAmax, leaf δ13C, and concentrations of chlorophyll a and b were identified as the most representative predictor variables for SFB, accounting for 73% of the variability in SFB. In conclusion, a combination of LAmax, leaf δ13C, and chlorophyll should be considered in selection programs for high-yield mulberry cultivars. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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Review

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19 pages, 1857 KiB  
Review
Coordination of Leaf Development Across Developmental Axes
by James W. Satterlee and Michael J. Scanlon
Plants 2019, 8(10), 433; https://doi.org/10.3390/plants8100433 - 22 Oct 2019
Cited by 21 | Viewed by 10088
Abstract
Leaves are initiated as lateral outgrowths from shoot apical meristems throughout the vegetative life of the plant. To achieve proper developmental patterning, cell-type specification and growth must occur in an organized fashion along the proximodistal (base-to-tip), mediolateral (central-to-edge), and adaxial–abaxial (top-bottom) axes of [...] Read more.
Leaves are initiated as lateral outgrowths from shoot apical meristems throughout the vegetative life of the plant. To achieve proper developmental patterning, cell-type specification and growth must occur in an organized fashion along the proximodistal (base-to-tip), mediolateral (central-to-edge), and adaxial–abaxial (top-bottom) axes of the developing leaf. Early studies of mutants with defects in patterning along multiple leaf axes suggested that patterning must be coordinated across developmental axes. Decades later, we now recognize that a highly complex and interconnected transcriptional network of patterning genes and hormones underlies leaf development. Here, we review the molecular genetic mechanisms by which leaf development is coordinated across leaf axes. Such coordination likely plays an important role in ensuring the reproducible phenotypic outcomes of leaf morphogenesis. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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13 pages, 641 KiB  
Review
Heterophylly: Phenotypic Plasticity of Leaf Shape in Aquatic and Amphibious Plants
by Gaojie Li, Shiqi Hu, Hongwei Hou and Seisuke Kimura
Plants 2019, 8(10), 420; https://doi.org/10.3390/plants8100420 - 16 Oct 2019
Cited by 50 | Viewed by 17831
Abstract
Leaves show great diversity in shape, size, and color in nature. Interestingly, many plant species have the ability to alter their leaf shape in response to their surrounding environment. This phenomenon is termed heterophylly, and is thought to be an adaptive feature to [...] Read more.
Leaves show great diversity in shape, size, and color in nature. Interestingly, many plant species have the ability to alter their leaf shape in response to their surrounding environment. This phenomenon is termed heterophylly, and is thought to be an adaptive feature to environmental heterogeneity in many cases. Heterophylly is widespread among land plants, and is especially dominant in aquatic and amphibious plants. Revealing the mechanisms underlying heterophylly would provide valuable insight into the interaction between environmental conditions and plant development. Here, we review the history and recent progress of research on heterophylly in aquatic and amphibious plants. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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30 pages, 1465 KiB  
Review
The Dynamic Genetic-Hormonal Regulatory Network Controlling the Trichome Development in Leaves
by Marco Fambrini and Claudio Pugliesi
Plants 2019, 8(8), 253; https://doi.org/10.3390/plants8080253 - 28 Jul 2019
Cited by 40 | Viewed by 7118
Abstract
Plant trichomes are outgrowths developed from an epidermal pavement cells of leaves and other organs. Trichomes (also called ‘hairs’) play well-recognized roles in defense against insect herbivores, forming a physical barrier that obstructs insect movement and mediating chemical defenses. In addition, trichomes can [...] Read more.
Plant trichomes are outgrowths developed from an epidermal pavement cells of leaves and other organs. Trichomes (also called ‘hairs’) play well-recognized roles in defense against insect herbivores, forming a physical barrier that obstructs insect movement and mediating chemical defenses. In addition, trichomes can act as a mechanosensory switch, transducing mechanical stimuli (e.g., insect movement) into physiological signals, helping the plant to respond to insect attacks. Hairs can also modulate plant responses to abiotic stresses, such as water loss, an excess of light and temperature, and reflect light to protect plants against UV radiation. The structure of trichomes is species-specific and this trait is generally related to their function. These outgrowths are easily analyzed and their origin represents an outstanding subject to study epidermal cell fate and patterning in plant organs. In leaves, the developmental control of the trichomatous complement has highlighted a regulatory network based on four fundamental elements: (i) genes that activate and/or modify the normal cell cycle of epidermal pavement cells (i.e., endoreduplication cycles); (ii) transcription factors that create an activator/repressor complex with a central role in determining cell fate, initiation, and differentiation of an epidermal cell in trichomes; (iii) evidence that underlines the interplay of the aforesaid complex with different classes of phytohormones; (iv) epigenetic mechanisms involved in trichome development. Here, we reviewed the role of genes in the development of trichomes, as well as the interaction between genes and hormones. Furthermore, we reported basic studies about the regulation of the cell cycle and the complexity of trichomes. Finally, this review focused on the epigenetic factors involved in the initiation and development of hairs, mainly on leaves. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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14 pages, 1669 KiB  
Review
The Diverse Roles of Auxin in Regulating Leaf Development
by Yuanyuan Xiong and Yuling Jiao
Plants 2019, 8(7), 243; https://doi.org/10.3390/plants8070243 - 23 Jul 2019
Cited by 54 | Viewed by 9909
Abstract
Leaves, the primary plant organs that function in photosynthesis and respiration, have highly organized, flat structures that vary within and among species. In recent years, it has become evident that auxin plays central roles in leaf development, including leaf initiation, blade formation, and [...] Read more.
Leaves, the primary plant organs that function in photosynthesis and respiration, have highly organized, flat structures that vary within and among species. In recent years, it has become evident that auxin plays central roles in leaf development, including leaf initiation, blade formation, and compound leaf patterning. In this review, we discuss how auxin maxima form to define leaf primordium formation. We summarize recent progress in understanding of how spatial auxin signaling promotes leaf blade formation. Finally, we discuss how spatial auxin transport and signaling regulate the patterning of compound leaves and leaf serration. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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Other

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8 pages, 1620 KiB  
Technical Note
CRISPR/Cas9-Mediated Mutagenesis of RCO in Cardamine hirsuta
by Claire Lessa Alvim Kamei, Bjorn Pieper, Stefan Laurent, Miltos Tsiantis and Peter Huijser
Plants 2020, 9(2), 268; https://doi.org/10.3390/plants9020268 - 18 Feb 2020
Cited by 1 | Viewed by 4021
Abstract
The small crucifer Cardamine hirsuta bears complex leaves divided into leaflets. This is in contrast to its relative, the reference plant Arabidopsis thaliana, which has simple leaves. Comparative studies between these species provide attractive opportunities to study the diversification of form. Here, [...] Read more.
The small crucifer Cardamine hirsuta bears complex leaves divided into leaflets. This is in contrast to its relative, the reference plant Arabidopsis thaliana, which has simple leaves. Comparative studies between these species provide attractive opportunities to study the diversification of form. Here, we report on the implementation of the CRISPR/Cas9 genome editing methodology in C. hirsuta and with it the generation of novel alleles in the RCO gene, which was previously shown to play a major role in the diversification of form between the two species. Thus, genome editing can now be deployed in C. hirsuta, thereby increasing its versatility as a model system to study gene function and evolution. Full article
(This article belongs to the Special Issue From Genes to Shape and Function: Leaf Morphogenesis at Play)
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