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Molecular Mechanisms of Leaf Morphogenesis

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 May 2020) | Viewed by 54196

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Special Issue Editor

Special Issue Information

Dear Colleagues,

Leaf morphology is obviously determined in a plant. By contrast, its morphology is often changeable when the plant copes with various environmental changes. We can speculate that leaf morphogenesis is based on the regulatory mechanisms with remarkable robustness and flexibility. Recent research has increasingly investigated the regulatory network of leaf morphogenesis and revealed some important regulators functioning in the leaf development but not obtained its full view of the molecular mechanisms of leaf morphogenesis.

To update our understanding of the leaf morphogenesis, this Special Issue will focus on the regulation of genes, proteins, hormones, and other metabolites for leaf morphogenesis in various plant species. It will further provide important insights in biochemical, developmental, and physiological events operating during morphogenesis. Emphasis will also be placed on the perspective views of how these molecular mechanisms contribute to the survival of plants and are applicable to improve plant traits.

Dr. Tomotsugu Koyama
Guest Editor

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Keywords

  • genes
  • leaf morphogenesis
  • metabolites
  • plant hormones
  • proteins
  • regulation

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Published Papers (9 papers)

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Research

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16 pages, 3723 KiB  
Article
Establishment of the Embryonic Shoot Meristem Involves Activation of Two Classes of Genes with Opposing Functions for Meristem Activities
by Mitsuhiro Aida, Yuka Tsubakimoto, Satoko Shimizu, Hiroyuki Ogisu, Masako Kamiya, Ryosuke Iwamoto, Seiji Takeda, Md Rezaul Karim, Masaharu Mizutani, Michael Lenhard and Masao Tasaka
Int. J. Mol. Sci. 2020, 21(16), 5864; https://doi.org/10.3390/ijms21165864 - 15 Aug 2020
Cited by 9 | Viewed by 4820
Abstract
The shoot meristem, a stem-cell-containing tissue initiated during plant embryogenesis, is responsible for continuous shoot organ production in postembryonic development. Although key regulatory factors including KNOX genes are responsible for stem cell maintenance in the shoot meristem, how the onset of such factors [...] Read more.
The shoot meristem, a stem-cell-containing tissue initiated during plant embryogenesis, is responsible for continuous shoot organ production in postembryonic development. Although key regulatory factors including KNOX genes are responsible for stem cell maintenance in the shoot meristem, how the onset of such factors is regulated during embryogenesis is elusive. Here, we present evidence that the two KNOX genes STM and KNAT6 together with the two other regulatory genes BLR and LAS are functionally important downstream genes of CUC1 and CUC2, which are a redundant pair of genes that specify the embryonic shoot organ boundary. Combined expression of STM with any of KNAT6, BLR, and LAS can efficiently rescue the defects of shoot meristem formation and/or separation of cotyledons in cuc1cuc2 double mutants. In addition, CUC1 and CUC2 are also required for the activation of KLU, a cytochrome P450-encoding gene known to restrict organ production, and KLU counteracts STM in the promotion of meristem activity, providing a possible balancing mechanism for shoot meristem maintenance. Together, these results establish the roles for CUC1 and CUC2 in coordinating the activation of two classes of genes with opposite effects on shoot meristem activity. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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16 pages, 4487 KiB  
Article
Transformation of Riccia fluitans, an Amphibious Liverwort Dynamically Responding to Environmental Changes
by Felix Althoff and Sabine Zachgo
Int. J. Mol. Sci. 2020, 21(15), 5410; https://doi.org/10.3390/ijms21155410 - 29 Jul 2020
Cited by 13 | Viewed by 7504
Abstract
The colonization of land by streptophyte algae, ancestors of embryophyte plants, was a fundamental event in the history of life on earth. Bryophytes are early diversifying land plants that mark the transition from freshwater to terrestrial ecosystems. The amphibious liverwort Riccia fluitans can [...] Read more.
The colonization of land by streptophyte algae, ancestors of embryophyte plants, was a fundamental event in the history of life on earth. Bryophytes are early diversifying land plants that mark the transition from freshwater to terrestrial ecosystems. The amphibious liverwort Riccia fluitans can thrive in aquatic and terrestrial environments and thus represents an ideal organism to investigate this major transition. Therefore, we aimed to establish a transformation protocol for R. fluitans to make it amenable for genetic analyses. An Agrobacterium transformation procedure using R. fluitans callus tissue allows to generate stably transformed plants within 10 weeks. Furthermore, for comprehensive studies spanning all life stages, we demonstrate that the switch from vegetative to reproductive development can be induced by both flooding and poor nutrient availability. Interestingly, a single R. fluitans plant can consecutively adapt to different growth environments and forms distinctive and reversible features of the thallus, photosynthetically active tissue that is thus functionally similar to leaves of vascular plants. The morphological plasticity affecting vegetative growth, air pore formation, and rhizoid development realized by one genotype in response to two different environments makes R. fluitans ideal to study the adaptive molecular mechanisms enabling the colonialization of land by aquatic plants. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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20 pages, 4974 KiB  
Article
Simple and Divided Leaves in Ferns: Exploring the Genetic Basis for Leaf Morphology Differences in the Genus Elaphoglossum (Dryopteridaceae)
by Alejandra Vasco and Barbara A. Ambrose
Int. J. Mol. Sci. 2020, 21(15), 5180; https://doi.org/10.3390/ijms21155180 - 22 Jul 2020
Cited by 15 | Viewed by 4925
Abstract
Despite the implications leaves have for life, their origin and development remain debated. Analyses across ferns and seed plants are fundamental to address the conservation or independent origins of megaphyllous leaf developmental mechanisms. Class I KNOX expression studies have been used to understand [...] Read more.
Despite the implications leaves have for life, their origin and development remain debated. Analyses across ferns and seed plants are fundamental to address the conservation or independent origins of megaphyllous leaf developmental mechanisms. Class I KNOX expression studies have been used to understand leaf development and, in ferns, have only been conducted in species with divided leaves. We performed expression analyses of the Class I KNOX and Histone H4 genes throughout the development of leaf primordia in two simple-leaved and one divided-leaved fern taxa. We found Class I KNOX are expressed (1) throughout young and early developing leaves of simple and divided-leaved ferns, (2) later into leaf development of divided-leaved species compared to simple-leaved species, and (3) at the leaf primordium apex and margins. H4 expression is similar in young leaf primordia of simple and divided leaves. Persistent Class I KNOX expression at the margins of divided leaf primordia compared with simple leaf primordia indicates that temporal and spatial patterns of Class I KNOX expression correlate with different fern leaf morphologies. However, our results also indicate that Class I KNOX expression alone is not sufficient to promote divided leaf development in ferns. Class I KNOX patterns of expression in fern leaves support the conservation of an independently recruited developmental mechanism for leaf dissection in megaphylls, the shoot-like nature of fern leaves compared with seed plant leaves, and the critical role marginal meristems play in fern leaf development. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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17 pages, 2751 KiB  
Article
Metabolomics Analysis Reveals Tissue-Specific Metabolite Compositions in Leaf Blade and Traps of Carnivorous Nepenthes Plants
by Alberto Dávila-Lara, Carlos E. Rodríguez-López, Sarah E. O'Connor and Axel Mithöfer
Int. J. Mol. Sci. 2020, 21(12), 4376; https://doi.org/10.3390/ijms21124376 - 19 Jun 2020
Cited by 13 | Viewed by 6805
Abstract
Nepenthes is a genus of carnivorous plants that evolved a pitfall trap, the pitcher, to catch and digest insect prey to obtain additional nutrients. Each pitcher is part of the whole leaf, together with a leaf blade. These two completely different parts of [...] Read more.
Nepenthes is a genus of carnivorous plants that evolved a pitfall trap, the pitcher, to catch and digest insect prey to obtain additional nutrients. Each pitcher is part of the whole leaf, together with a leaf blade. These two completely different parts of the same organ were studied separately in a non-targeted metabolomics approach in Nepenthes x ventrata, a robust natural hybrid. The first aim was the analysis and profiling of small (50–1000 m/z) polar and non-polar molecules to find a characteristic metabolite pattern for the particular tissues. Second, the impact of insect feeding on the metabolome of the pitcher and leaf blade was studied. Using UPLC-ESI-qTOF and cheminformatics, about 2000 features (MS/MS events) were detected in the two tissues. They showed a huge chemical diversity, harboring classes of chemical substances that significantly discriminate these tissues. Among the common constituents of N. x ventrata are phenolics, flavonoids and naphthoquinones, namely plumbagin, a characteristic compound for carnivorous Nepenthales, and many yet-unknown compounds. Upon insect feeding, only in pitchers in the polar compounds fraction, small but significant differences could be detected. By further integrating information with cheminformatics approaches, we provide and discuss evidence that the metabolite composition of the tissues can point to their function. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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13 pages, 2444 KiB  
Article
Class I KNOX Is Related to Determinacy during the Leaf Development of the Fern Mickelia scandens (Dryopteridaceae)
by Rafael Cruz, Gladys F. A. Melo-de-Pinna, Alejandra Vasco, Jefferson Prado and Barbara A. Ambrose
Int. J. Mol. Sci. 2020, 21(12), 4295; https://doi.org/10.3390/ijms21124295 - 16 Jun 2020
Cited by 18 | Viewed by 4038
Abstract
Unlike seed plants, ferns leaves are considered to be structures with delayed determinacy, with a leaf apical meristem similar to the shoot apical meristems. To better understand the meristematic organization during leaf development and determinacy control, we analyzed the cell divisions and expression [...] Read more.
Unlike seed plants, ferns leaves are considered to be structures with delayed determinacy, with a leaf apical meristem similar to the shoot apical meristems. To better understand the meristematic organization during leaf development and determinacy control, we analyzed the cell divisions and expression of Class I KNOX genes in Mickelia scandens, a fern that produces larger leaves with more pinnae in its climbing form than in its terrestrial form. We performed anatomical, in situ hybridization, and qRT-PCR experiments with histone H4 (cell division marker) and Class I KNOX genes. We found that Class I KNOX genes are expressed in shoot apical meristems, leaf apical meristems, and pinnae primordia. During early development, cell divisions occur in the most distal regions of the analyzed structures, including pinnae, and are not restricted to apical cells. Fern leaves and pinnae bear apical meristems that may partially act as indeterminate shoots, supporting the hypothesis of homology between shoots and leaves. Class I KNOX expression is correlated with indeterminacy in the apex and leaf of ferns, suggesting a conserved function for these genes in euphyllophytes with compound leaves. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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Review

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11 pages, 1464 KiB  
Review
Recent Progress Regarding the Molecular Aspects of Insect Gall Formation
by Seiji Takeda, Tomoko Hirano, Issei Ohshima and Masa H. Sato
Int. J. Mol. Sci. 2021, 22(17), 9424; https://doi.org/10.3390/ijms22179424 - 30 Aug 2021
Cited by 22 | Viewed by 5558
Abstract
Galls are characteristic plant structures formed by cell size enlargement and/or cell proliferation induced by parasitic or pathogenic organisms. Insects are a major inducer of galls, and insect galls can occur on plant leaves, stems, floral buds, flowers, fruits, or roots. Many of [...] Read more.
Galls are characteristic plant structures formed by cell size enlargement and/or cell proliferation induced by parasitic or pathogenic organisms. Insects are a major inducer of galls, and insect galls can occur on plant leaves, stems, floral buds, flowers, fruits, or roots. Many of these exhibit unique shapes, providing shelter and nutrients to insects. To form unique gall structures, gall-inducing insects are believed to secrete certain effector molecules and hijack host developmental programs. However, the molecular mechanisms of insect gall induction and development remain largely unknown due to the difficulties associated with the study of non-model plants in the wild. Recent advances in next-generation sequencing have allowed us to determine the biological processes in non-model organisms, including gall-inducing insects and their host plants. In this review, we first summarize the adaptive significance of galls for insects and plants. Thereafter, we summarize recent progress regarding the molecular aspects of insect gall formation. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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19 pages, 2749 KiB  
Review
Roles of ASYMMETRIC LEAVES2 (AS2) and Nucleolar Proteins in the Adaxial–Abaxial Polarity Specification at the Perinucleolar Region in Arabidopsis
by Hidekazu Iwakawa, Hiro Takahashi, Yasunori Machida and Chiyoko Machida
Int. J. Mol. Sci. 2020, 21(19), 7314; https://doi.org/10.3390/ijms21197314 - 3 Oct 2020
Cited by 13 | Viewed by 7320
Abstract
Leaves of Arabidopsis develop from a shoot apical meristem grow along three (proximal–distal, adaxial–abaxial, and medial–lateral) axes and form a flat symmetric architecture. ASYMMETRIC LEAVES2 (AS2), a key regulator for leaf adaxial–abaxial partitioning, encodes a plant-specific nuclear protein and directly represses [...] Read more.
Leaves of Arabidopsis develop from a shoot apical meristem grow along three (proximal–distal, adaxial–abaxial, and medial–lateral) axes and form a flat symmetric architecture. ASYMMETRIC LEAVES2 (AS2), a key regulator for leaf adaxial–abaxial partitioning, encodes a plant-specific nuclear protein and directly represses the abaxial-determining gene ETTIN/AUXIN RESPONSE FACTOR3 (ETT/ARF3). How AS2 could act as a critical regulator, however, has yet to be demonstrated, although it might play an epigenetic role. Here, we summarize the current understandings of the genetic, molecular, and cellular functions of AS2. A characteristic genetic feature of AS2 is the presence of a number of (about 60) modifier genes, mutations of which enhance the leaf abnormalities of as2. Although genes for proteins that are involved in diverse cellular processes are known as modifiers, it has recently become clear that many modifier proteins, such as NUCLEOLIN1 (NUC1) and RNA HELICASE10 (RH10), are localized in the nucleolus. Some modifiers including ribosomal proteins are also members of the small subunit processome (SSUP). In addition, AS2 forms perinucleolar bodies partially colocalizing with chromocenters that include the condensed inactive 45S ribosomal RNA genes. AS2 participates in maintaining CpG methylation in specific exons of ETT/ARF3. NUC1 and RH10 genes are also involved in maintaining the CpG methylation levels and repressing ETT/ARF3 transcript levels. AS2 and nucleolus-localizing modifiers might cooperatively repress ETT/ARF3 to develop symmetric flat leaves. These results raise the possibility of a nucleolus-related epigenetic repression system operating for developmental genes unique to plants and predict that AS2 could be a molecule with novel functions that cannot be explained by the conventional concept of transcription factors. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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18 pages, 1610 KiB  
Review
Synergistic Interaction of Phytohormones in Determining Leaf Angle in Crops
by Xi Li, Pingfan Wu, Ying Lu, Shaoying Guo, Zhuojun Zhong, Rongxin Shen and Qingjun Xie
Int. J. Mol. Sci. 2020, 21(14), 5052; https://doi.org/10.3390/ijms21145052 - 17 Jul 2020
Cited by 34 | Viewed by 6478
Abstract
Leaf angle (LA), defined as the angle between the plant stem and leaf adaxial side of the blade, generally shapes the plant architecture into a loosen or dense structure, and thus influences the light interception and competition between neighboring plants in natural settings, [...] Read more.
Leaf angle (LA), defined as the angle between the plant stem and leaf adaxial side of the blade, generally shapes the plant architecture into a loosen or dense structure, and thus influences the light interception and competition between neighboring plants in natural settings, ultimately contributing to the crop yield and productivity. It has been elucidated that brassinosteroid (BR) plays a dominant role in determining LA, and other phytohormones also positively or negatively participate in regulating LA. Accumulating evidences have revealed that these phytohormones interact with each other in modulating various biological processes. However, the comprehensive discussion of how the phytohormones and their interaction involved in shaping LA is relatively lack. Here, we intend to summarize the advances in the LA regulation mediated by the phytohormones and their crosstalk in different plant species, mainly in rice and maize, hopefully providing further insights into the genetic manipulation of LA trait in crop breeding and improvement in regarding to overcoming the challenge from the continuous demands for food under limited arable land area. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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17 pages, 1949 KiB  
Review
The Regulation of CIN-like TCP Transcription Factors
by Jingqiu Lan and Genji Qin
Int. J. Mol. Sci. 2020, 21(12), 4498; https://doi.org/10.3390/ijms21124498 - 24 Jun 2020
Cited by 40 | Viewed by 5734
Abstract
TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR 1 and 2 (TCP) family proteins are the plant-specific transcription factors extensively participating in diverse developmental processes by integrating external cues with internal signals. The roles of CINCINNATA (CIN)-like TCPs are conserved in control of the morphology and size [...] Read more.
TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR 1 and 2 (TCP) family proteins are the plant-specific transcription factors extensively participating in diverse developmental processes by integrating external cues with internal signals. The roles of CINCINNATA (CIN)-like TCPs are conserved in control of the morphology and size of leaves, petal development, trichome formation and plant flowering. The tight regulation of CIN-like TCP activity at transcriptional and post-transcriptional levels are central for plant developmental plasticity in response to the ever-changing environmental conditions. In this review, we summarize recent progresses with regard to the function and regulation of CIN-like TCPs. CIN-like TCPs are regulated by abiotic and biotic cues including light, temperature and pathogens. They are also finely controlled by microRNA319 (miRNA319), chromatin remodeling complexes and auxin homeostasis. The protein degradation plays critical roles in tightly controlling the activity of CIN-like TCPs as well. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Leaf Morphogenesis)
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