Next Article in Journal
Remote Sensing-Based Land Suitability Analysis for Forest Restoration in Madagascar
Next Article in Special Issue
Variation Pattern and Genome-Wide Association Study of Leaf Phenotypic Traits among Ancient Ginkgo biloba L. Populations
Previous Article in Journal
Biomass Estimation and Carbon Storage of Taxodium Hybrid Zhongshanshan Plantations in the Yangtze River Basin
Previous Article in Special Issue
Chloroplast Genome Variation and Phylogenetic Analyses of Seven Dwarf Ornamental Bamboo Species
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 13
Issue 10
10.3390/f13101726
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Formation of Shapes: Interplay of Genes during Leaf Development Processes

by
Jikai Ma
1,2 and
Huogen Li
2,*
1
College of Forestry, Jiangxi Agriculture University, Nanchang 330045, China
2
College of Forestry, Nanjing Forestry University, Nanjing 210037, China
*
Author to whom correspondence should be addressed.
Forests 2022, 13(10), 1726; https://doi.org/10.3390/f13101726
Submission received: 15 August 2022 / Revised: 14 October 2022 / Accepted: 17 October 2022 / Published: 20 October 2022
(This article belongs to the Special Issue Population Genetic and Morphological Diversity of Woody Plants)
Browse Figures
Versions Notes

Abstract

:
Leaf shape, as one of the clearest manifestations of plant morphology, shows considerable variation owing to genetics and the environment. Leaf initiation occurs in the peripheral zone of the SAM and goes through the three overlapping phases of leaf primordium initiation, leaf dorsiventral development, and leaf marginal meristem establishment. Transcription factors, such as KNOX, WOX, and CUC; hormone-regulating genes, such as GA2ox, GA20ox, and PIN1; and miRNAs such as miR164/165 are tightly involved in leaf shaping through the generation of intricate cooperative networks in different temporal phases and specific tissue zones. Here, we briefly discuss the critical interplay occurring between certain genes and the pivotal role these play in the leaf developmental network and phytohormone regulation, including AS1/AS2–KNOX–GA20ox–GA, miR164–NAM/CUC–PIN1–auxin, and CUC–BAS1/CYP734A–BR, and we attempt to summarize several basic insights into the mechanisms of leaf shape regulation.

1. Introduction

Leaf morphology is a notable part of plant morphology exhibiting tremendous diversity for most plants [1]. As we know, the leaf has profound significance for photosynthesis, respiration, and photoperception [2]. As a solar panel, the leaf has to capture solar energy, which is required for photosynthesis to maintain growth and development [3]. Leaf shape has a relevant impact on the efficiency of light capture and heat dissipation and can reflect how plants have adapted to their climates [4,5]. For instance, Serratula tinctoria L. (Asteraceae) has vigorous vertical growth under limited light conditions and develops extensively lobed leaves due to shading from its competitors [6]. Moreover, a leaf’s hydraulic resistance is negatively correlated with its lobes, since deep lobes may promote water balance in dry atmospheres, as shown in Quercus L. (Fagaceae) [7]. Generally, leaf shape and size are essential factors that partially govern angiosperm growth [8]. Leaf shape can be manipulated by genetic and environmental factors. For example, North American lake cress (Rorippa aquatica (Eaton) E.J.Palmer et Steyerm., of the family Brassicaceae), is a typical example of heterophylly in which leaves with a variety of shapes and sizes grow on the same plant, bearing simple leaves on land but pinnately divided leaves in submerged conditions [9]. Indeed, this heterophylly is altered by the induction of the KNOX–GA module [10]. Essentially, KNOX and BELL are two types of TALE TF that control meristem formation and maintenance, organ morphogenesis, organ position, and several aspects of the reproductive phase [11]. Members of the class 1 KNOX family (KNOXI), in particular, are critical in the maintenance of the shoot apical meristem and contribute to leaf dissection and complex morphology through hormone regulation [12,13,14,15,16,17,18,19,20,21,22,23]. In the Brassicaceae family, the RCO homeodomain protein plays a pivotal role in determining leaf complexity [13,24]. In C. hirsuta (Cardamine hirsuta L., family Brassicaceae), RCO goes through gene duplication and neofunctionalization, increasing leaf complexity, but this is evolutionarily lost in A. thaliana (Arabidopsis thaliana (L.) Heynh., family Brassicaceae), resulting in simple leaf morphology [24].
Leaf initiation begins with a group of cells around the flank of the SAM, which is the growth region in plants found within the tips of the shoots. At the beginning of leaf initiation in the SAM, the TALE TFs play remarkable roles in SAM maintenance and serve as the pluripotent regulators of the corresponding gene network. This group includes the GA20ox, GA2ox, and PIN1 hormonal regulators [23,25,26,27]. Furthermore, several TF, such as AS1 and CUC1-3, are involved in leaf development. As a model plant, Arabidopsis Heynh. has been well-studied in the field of leaf development. In the regulatory interplay occurring upstream of KNOX, AS1, a MYB TF, and AS2 belonging to the LOB family interact with LHP1 to repress KNOX genes in Arabidopsis [28]. AS1 also combines with auxin activities to regulate KNAT1/BP, a prominent KNOXI gene, promoting leaf development [29]. Furthermore, CUC genes act as key factors in the gene network involved in the development of the leaf margin. KNOXI genes can coordinate with CUC genes and hormonal regulatory genes to balance cell differentiation and proliferation, facilitating leaf lobes in Arabidopsis [12,30]. Along with leaf emergence, the CUC genes are critical regulators that cooperate in these genetic interplays, including interactions with hormonal factors such as the PIN protein, transcriptional factors such as KNOX, and microRNA such as miRNA164a. These regulators act to promote sinus formation at the leaf margin [31]. It has been reported that inactivating the CUC3 gene partially suppresses serrations at the leaf margin in A. thaliana [16,32].
There are many factors that play indispensable roles in different phases of leaf development, which is profoundly controlled by these factors in determining the final shape. Even though many works have referred to leaf development and morphogenesis in retrospect, a comprehensive understanding of the mechanisms of leaf shaping is lacking, and further work in this regard is required. Here, we concisely review a few studies of leaf development and discuss these regulations with the main focus on the roles of genes, such as KNOX and CUC, from leaf initiation to the development of the entire leaf, referring to model networks of regulation.

2. Leaf Initiation and Morphogenesis

2.1. Where Does Leaf Initiation Occur?

In seed plants, the SAM is the basic unit of plant development incorporating the leaves, stem, and shoot, and regulatory mechanisms also occur within this dynamic structure [33]. The SAM has the dual function of maintaining an active stem cell population while concurrently generating new organs [34]. The organs form as primordia on the meristem flanks, whereas the self-renewing stem cell reservoir at the apex replenishes the cells that depart from the meristem into primordia including leaf primordia.

2.2. How Is a Leaf Shaped?

The early events of leaf initiation are similar across angiosperms [35]. Once leaf initiation begins from the SAM, it continuously progresses through three overlapping phases: leaf primordium initiation, the establishment of dorsiventrality, and the development of a marginal meristem [2,33]. These events generally lead a group of cells to form an entire leaf [2,33,36]. Additionally, there are three axes of growth in the establishment of a leaf: adaxial–abaxial, proximal–distal, and medial–lateral [37,38,39]. The leaf expands along these three axes and undergoes determinate growth, during which time the basic shape and potential size of the leaf are determined, and the organogenesis of the lateral appendages occurs [37,38,40]. The leaf’s final shape depends on the cooperation of two growth modes, namely a conserved organ-wide growth mode that reflects differentiation and a local, directional mode involving the patterning of growth foci along with the leaf margin [22].

3. Molecular Regulation of Leaf Development

In spite of growing on the same individual plant, there are no two completely identical leaves, mainly because of the impacts of external factors from the environment and the internal factors from the plant’s genetics.

3.1. Regulation in Early Developmental Events: Leaf Initiation and Development

Prior to leaf emergence, there are interplays between a broad number of genes within the SAM through interactions and collaborations and established networks of leaf development. Previous studies have suggested that cell cycling associated with leaf morphogenesis patterns of cell proliferation and differentiation occurs concurrently during leaf development [41,42]. Leaf initiation from the SAM involves a balance between cell proliferation and the generation of primordia. These processes are regulated by a great number of genes, such as the KNOX genes [35,43,44]. SAM maintenance and leaf development require a balance between pluripotent and differentiated cells, and there are multitudinous genes involved in meristem regulatory activity [37].

3.1.1. Regulation of KNOX

KNOXIs are expressed during the early leaf developmental events in the SAM and are essential for SAM formation and maintenance [45]. STM, a KNOXI gene, is locally downregulated during leaf primordia development [46,47,48]. The mutations of stm and the loss of function of KNOX lead to a failure to form the undifferentiated cells of the shoot meristem during embryonic development [49,50]. The ectopic expression of KNAT1 induces all leaves to become lobed [51]. Additionally, the ectopic expression of the rice OSH, a KNOXI gene, interferes with the development of leaf blades and maintains leaves in less differentiated states [52]. In fact, KNOX genes were first found in maize, and they can be classified into two subclasses based on sequence similarity within the homeodomain, intron locations, expression pattern, and phylogenetic analysis [53,54,55,56]. On the one hand, KNOXI genes, including KNAT1/BP, KNAT2, KNAT6, and STM in Arabidopsis, are characteristically expressed in the meristem and stem, but their expression is downregulated in the leaf primordia of most simple leaf species [57]. On the other hand, previous studies have shown that in plant organs, there is a more widespread expression of class 2 KNOX (KNOXII) genes than of KNOXI genes, which indicates that they might have different functions [53,58,59]. Conversely, KNOXI genes can be expressed in the leaf primordia of dissected leaf plants, which implies that they may be involved in leaf diversity. Even if the KNOXII genes are barely involved in leaf shape regulation, they are extremely important for the regulation of other processes, which is a critical point when considering the classification of KNOXI and KNOXII genes. For example, KNOX4, a member of the KNOXII class, controls physical dormancy by regulating seed-coat cuticle development in Medicago truncatula Gaertn. (Fabaceae) [60]. Moreover, the KNOXII members KNAT3 and KNAT7 can work cooperatively to influence secondary cell wall deposition [61].

3.1.2. The Upstream Regulation of KNOX

The KNOX genes can be mediated by several genes, including AS1, AS2, BOP1, and BOP2 genes in the meristem (Figure 1b). Previous studies have shown that as1 mutations lead to marginal outgrowths or lobes at blades in Arabidopsis [62,63,64,65]. In fact, the leaf phenotype of the as2 mutant is similar to that of the as1 mutant in that KNOX genes are aberrantly expressed [63,64,66,67]. In addition to phenotypic similarities between as1/as2 and KNOX over- or aberrant expressors, genetic analysis has demonstrated KNOX-mediated as1/as2 phenotypes [67]. AS1 has been identified as negatively mediating the KNOXI genes KNAT1 and KNAT2, whereas STM negatively represses AS1 [62]. Moreover, AS1 and AS2 complexes can facilitate the generation of H3K27me3 modifications in the chromatin regions of KNAT1 and KNAT2 to facilitate direct interaction with LHP1 (Figure 1b) [28]. The complex can bind to the regulatory motifs CWGTTD and KMKTTGAHW, which are present at two sites in the promoters of KNOX targets immediately upstream and surrounding an enhancer region required for expression in developing leaves [68]. The complex is required for stable KNOX gene silencing and can lead to the formation of a stable repressive chromatin state that blocks enhancer activity throughout leaf development. In addition, it is critical that BOP1 and BOP2, both encoding an organ-specific BTB–POZ domain protein, can mediate leaf morphogenesis and patterning by directly activating AS2 transcription and generating conditions for KNOX repression at the leaf base [69,70,71].

3.1.3. Gibberellin Regulation by KNOX

Gibberellin regulation by KNOX takes the form of the net repression of the active GA level to maintain SAM activity [72] (Figure 1b). GA20ox and GA2ox are two key genes involved in GA biosynthesis regulated by KNOX proteins. Genetic studies have shown that KNOXI proteins can bind to TGAC sequences, especially including specific cis regulators in vitro, and four specific cis-regulatory elements recognized by KNOX proteins have been identified as having the TGAC sequence. In tobacco, NTH15 is mainly expressed in the leaf primordia and young leaves, and its protein strongly binds to GTGAC, a 5 bp dyad symmetric sequence in the first intron of Ntc12, which encodes the GA 20-oxidase enzyme and leads to decreased GA biosynthesis [73,74,75]. In the potato, StBEL5 and POTH1 interact with TALE proteins in binding to the ga20ox1 promoter through two TGAC cores [76]. Previous research has also indicated that the KNOX protein can bind to an intron of ga2ox1 through a cis-regulatory element containing two TGAC motifs in maize [77].

3.1.4. Cytokinin Regulation by KNOX

CK biosynthesis is required alongside KNOX activity. KNOX proteins maintain SAM function, establishing a zone with increased CK and depressed GA activity for meristem maintenance (Figure 1b) [27]. In rice, KNOX proteins decrease GA biosynthesis while elevating CK biosynthesis through OsIPT2 and OsIPT3, two CK biosynthesis genes that maintain the high-CK and resulting low-GA context needed for meristem formation and maintenance [78].

3.1.5. Brassinosteroid Regulation by CUC

BRs are a class of steroid hormones that are essential for differentiation in plants [79,80,81]. In BR-hypersensitive mutants, organ fusion occurs [82]. BRs are involved in organ boundary formation and are regulated by organ boundary identity genes. BZR1, a BR-activated nuclear protein, directly represses CUC, the organ boundary identity gene (Figure 1c). In rice, CYP734A2, CYP734A4, and CYP734A6, which encode BR catabolism enzymes, are upregulated through OSH1 gene induction, whereas OSH1 loss of function mutants have boundary defects in leaves and in SAM, which leads to a BR-overproduction phenotype [82,83,84,85].

3.1.6. Auxin Transported by PIN

The auxin phytohormone is one of the most crucial factors regulating plant organ formation, especially leaf development. Generally, auxin is transported by PIN1-dependent efflux; however, it must act together with AS1 to repress BP expression to promote leaf development and outgrowth at the flanks of the SAM [29,86]. Furthermore, leaf initiation can generate auxin, and it can be depleted from the proximity region via the PIN auxin efflux transporter, thereby inhibiting additional leaf primordium initiation at the SAM periphery [86,87,88] (Figure 1b). The auxin is transported back to the meristem under epidermal PIN1 polarity to stimulate the leaf and the leaf primordium to produce auxin [48,86,88]. Recently, it was reported that a WOX–auxin regulatory module determines the formation of leaf shape by coordinating growth along the proximodistal and mediolateral leaf axes [89].

3.1.7. Interplay between KNOX and CUC

The CUC genes encoding NAC TFs contribute to organ boundary formation, especially between lateral organs and the SAM [90]. The double mutant of cuc1 and cuc2 exhibits cotyledon fusion on both sides and has an obvious lack of SAM defects. Similarly, stm mutants also display a loss of SAM phenotype but show weak cotyledon fusion. The CUC/STM regulatory pathway is critical for the establishment of the boundary between the cotyledons and for the initiation of the SAM [91]. CUC1 was shown to be regulated by KNOX binding sites in its promoter [30]. CUC genes are required for STM expression and are involved in SAM formation and processes at the shoot organ boundary (Figure 1b) [46,90,92,93].

3.1.8. Regulation of Other Genes in the SAM

The CLV–WUS feedback signaling interaction maintains the pluripotency of stem cells and coordinates their cell proliferation and differentiation in the SAM (Figure 1a) [94]. The WUS gene encodes a transcription factor with a homeobox domain and is expressed in the stem-end meristem tissue. When WUS protein translation is completed, it will gradually migrate to the upper three layers of cells in the central region and directly bind to the 1080 bp upstream of the CLV gene promoter to activate the expression of the CLV3 gene, and CLV can move back to the organizing center to inhibit WUS expression [95,96]. Furthermore, KNOXs, especially STM, act as indispensable regulators in the SAM. The main function of STM is to inhibit cell differentiation and maintain the undifferentiated state of some cells in the SAM. CLV gene expression regulation is also influenced by STM and WUSWUS [97]. STM is required to suppress differentiation throughout the meristem dome, and these two processes sustain the maintenance and formation of the SAM. STM has converse functions to CLV, and undifferentiated cells of the shoot meristem fail to form in stm mutants. Overall, CLV and STM play relevant but opposing roles in the regulation of cell division or cell differentiation in meristems [50].
To maintain SAM function, KNOX genes serve as versatile factors regulating downstream genes, especially the plant phytohormonal regulatory factors [10,23,27,72,73,74,76,77,85,86,98]. The interplays between genes are maintained in early leaf primordium development along the adaxial–abaxial axis (Figure 1a).

3.2. Axial Polar Growth Regulation

3.2.1. Adaxial–Abaxial Establishment Regulation

If the primordia lose adaxial–abaxial development, they will produce a terete or stick-like leaf organ but barely shape an entire lamina. Leaving the SAM behind, as noted above, the primordia develop along three axes. Indeed, leaf adaxial fate is determined by the activity of a few gene products including PHV, PHB, and REV of HD-ZIP III [99,100]. The miR165/166, which acts in the abaxial domain of the leaf primordium, can target HD-ZIP III mRNAs [101]. Conversely, HD-ZIP III genes interact with HD-ZIP II genes to repress miR165/166 [102,103]. In addition, AS2 is directly repressed in the adaxial region by KANADI (KAN), a nuclear-localized protein in the GARP [104,105] (Figure 1c). Additionally, BOP2 is indispensable for AS2 activation, specifically in the proximal, adaxial zone of the leaf [69,71].
Additionally, leaf abaxial fate is controlled by KAN, which governs the abaxial fate together with the YABBY (YAB) TF and ETT/ARF3-ARF4 [86,99,104,106,107,108]. The mutations of ETT/ARF3-ARF4 have been found to alleviate ectopic KAN activity [109]. Three ARF genes, ARF2, ETT, and ARF4, have been identified as targets by the trans-acting siRNA (ta-siRNAs/TAS)3 (Figure 1c) [108,110,111]. Moreover, HD-ZIP III and KANADI mutants exhibit complementary phenotypes in A. thaliana [99].

3.2.2. Leaf Blade Formation

Leaf size is largely contingent on the plant species but varies, to a certain extent, due to environmental factors [112,113,114,115]. It has been reported that leaf size is partially mediated by overlapping pathways involving AS2, CIN encoding TCP TF, and hormone dynamics. There are two classes of adverse function factors in charge of the switch balance between cell expansion and cell proliferation: class II TCP, which negatively regulates leaf growth, and the GRF, whose overexpression often results in a larger leaf size [116,117]. The size of the proliferative region at the leaf base seems to be enlarged, and mutants with a loss of function of CIN have a concave distal boundary, such that cells at the leaf margin still proliferate, whereas cells in the center are already inhibited from proliferation [118,119]. Furthermore, ARP (AS1/RS2/PHAN), a MYB domain TF, is named by the AS1 of Arabidopsis, the RS2 of maize, and the PHAN of Antirrhinum L., three homologous proteins. ARP and AS2 also can manipulate the development of a symmetrical polarity of lamina expansion [62,120,121,122,123]. AS1/AS2 may directly inhibit KNOXI gene expression to enhance leaf primordia initiation at the SAM flank [124]. Furthermore, AS1/AS2 promotes leaf development by regulating the dorsoventral axis of leaf primordia initiation of organ formation [125].

3.3. Patterning Determination: Leaf Complexity

Leaf morphology can be classified as simple or dissected, whereas different types of leaves may recruit different factors and undergo different pathways in generating the final leaf shape. In C. hirsuta, a dissected leaf species, ChBP is repressed by the miR164A/ChCUC module and ChAS1, but this interaction never occurs in A. thaliana, a simple leaf species [12]. KNOX activity is under the control of different cis-regulatory factors in leaf primordia development, which induce leaflet formation [126]. The cis-regulatory factors of KNOX have significant roles in determining leaf complexity [127]. Additionally, the HBs, which contain a conserved 60 amino acid motif TF, contribute substantially to controlling leaf complexity. As mentioned above, KNOXI genes are expressed in the primordia of dissected leaves but are downregulated in the primordia of simple leaves, which indicates that different pathways are regulated by KNOXI genes in simple and dissected leaves. A. thaliana, which has simple leaves, and C. hirsuta, which has dissected leaves, are classic examples used in the study of simple dissected leaf diversity. In C. hirsuta, KNOX proteins are indispensable in the leaf, as they delay cellular differentiation, resulting in the development of dissected leaves, whereas in A. thaliana, they are excluded from leaves, leading to the generation of simple leaves [127]. In addition to the KNOX, RCO, encoding the homeodomain protein, has also been specifically identified as being involved in leaf complexity, and its patterns of expression enhance C. hirsuta leaf complexity by repressing growth at the flanks as well as leaflet formation [13]. However, STM/BP-like genes are uncoupled from PHAN in M. truncatula. Moreover, KNOXI and SGL1, which is an LFY ortholog, regulate parallel pathways of leaf development in M. truncatula [124].

3.4. The Elaboration of the Edge: Leaf Margins

Whether a leaf shape is simple or dissected, the leaf margin can be characterized as entire (smoothed), serrated, or lobed [33]. Members of the NAM/CUC family, which encode large evolutionarily conserved NAC proteins, are also involved in organ initiation and delimitation [90,128,129]. Notably, a collaborative group of CUC genes has been explored in different species with lobed and dissected leaves: Aquilegia caerulea E.James (Ranunculaceae), C. hirsuta, Pisum sativum L. (Fabaceae), Solanum lycopersicum L. (Solanaceae), and S. tuberosum L. [130]. The formation of the leaf margin mediated by a small gene regulatory network including miR164 and CUC/NAM genes and auxin activity components establishes a miR164–CUC/NAM–PIN–auxin module, which has been demonstrated to play a role in leaf serration [12,32,130,131]. Recent genetic studies resulted in the revelation of an elegant module in elucidating the mechanism underlying the development regulation of leaf shape, which includes two loops at the leaf margin [131]. The first loop requires PIN1 auxin efflux transporters to capture potential auxins with self-organizing patterns in diverse developmental contexts. The other loop depends on CUC2, which facilitates the PIN1-dependent generation of auxin maxima activity. For instance, the serration development is driven by interspersed active peaks of growth-promoting auxin and CUC2 [131]. The coordination between CUC2 and miR164a determines the extent of serration. The mutations of the miR164a gene enhance serration at the leaf margin, and the overexpression of miR164 promotes the smoothness of the leaf margin in A. thaliana. It is certain that deep serrations are extensively governed by interaction with miR164-resistant CUC2 [132]. While CUC2 interacts early with miR164 at the commencement of tooth development, CUC3 is prone to sustaining serrated tooth outgrowth (Figure 2). The CUC3 gene functions in partially suppressing leaf serration [16]. However, as long as CUC2 is uniformly expressed along the leaf margin instead of discretely expressed at the teeth, a smooth leaf margin will be generated, replacing the serrated margin of the leaf. At the dissected leaf margin, NAM/CUC genes establish a boundary domain that delimits leaflets and has a dual role in locally promoting leaflet separation [130]. Furthermore, the KNOXI proteins facilitate leaflet initiation in dissected leaf plants, and the actions of KNOX proteins depend on the ability of the PIN1 auxin efflux transporter to organize auxin [133]. KNOX activity inhibits cellular differentiation, leading to the production of dissected leaves in C. hirsuta [127]. Additionally, the ectopic expression of KNOX in leaves can perturb PIN1-dependent local gradients, thereby influencing auxin activity and resulting in leaf lobe or leaflet outgrowth promotion (Figure 2) [29].

4. Further Perspectives and Conclusions

Leaf shape is one of the most valuable traits for studying plants. Despite important studies having been conducted on a few model plants, there are still many plant species with possibly different leaf shape regulatory mechanisms that have played significant roles in plant evolution and, therefore, require further research. Furthermore, some genetic networks are still not yet fully elucidated, i.e., the precise domains in which genes impact their target genes and the regulatory balance in developmental phases have not been determined.
Here, we briefly summarized the leaf formation process to present the genes involved in leaf shaping and describe their roles throughout dynamic and overlapping phases. In each special phase, we attempted to concentrate on several core genes as the key players in that specific phase. For example, the KNOXI genes serve as a pivotal component contributing to the coordination of up/downstream genes in the SAM. Indeed, the genetics of leaf morphology shaping processes comprise enormous networks, and we concisely presented the details of the interplay between a few genetic elements associated with leaf shaping processes, such as NAM/CUC–mi164a–PIN1–auxin, KNOX–GA20ox/GA2ox–GA, and KNOX–BAS1/CYP734A–BR.

Author Contributions

Conceptualization, J.M. and H.L.; writing—original draft preparation, J.M.; writing—review and editing, J.M. and H.L.; supervision, H.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (grant number 31770718).

Acknowledgments

We are thankful for funding from the National Natural Science Foundation of China (31770718) and three anonymous reviewers for inspiring comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

ARFAUXIN RESPONSE FACTOR
ARPAS1/RS2/PHAN
AS1ASYMMETRIC LEAVES1
BLHBEL1-like homeobox
BOP1BLADE ON PETIOLE1
BPBREVIPEDICELLUS
BRsBrassinosteroids
BZR1Brassinazole-resistant 1
CINCINCINNATA
CKCytokinin
CLVCLAVATA
CUCCUP-SHAPED COTYLEDON
CYP734Cytochrome P450 family 734
ETTETTIN
GA20oxGIBBERELLIN 20 OXIDASE
GA2oxGIBBERELLIN 2 OXIDASE
GARPGLUTAMIC ACID-RICH PROTEIN
GRFGROWTH REGULATING FACTOR
H3K27me3histone H3 lysine 27 trimethylation
HD-ZIPHomeodomain leucine zipper
KANKANADI
KNATKNOTTED-like HOMEOBOX Arabidopsis thaliana
KNOXKNOTTED-like HOMEOBOX
LHP1LIKE HETEROCHROMATIN PROTEIN 1
LOBLATERAL ORGAN BOUNDARIES
miRNAmicroRNA
NTH15Nicotiana tabacum homeobox15
OSHOryza sativa homeobox
OsIPTOryza sativa isopentenyl transferases
PHANPHANTASTICA
PHBPHABULOSA
PHVPHAVOLUTA
PIN1PIN-FORMED1
POTH1potato homeobox1
RCOREDUCED COMPLEXITY
REVREVOLUTA
RS2ROUGH SHEATH2
SAMshoot apical meristem
SGL1SINGLE LEAFLET1
StBEL5Solanum tuberosom BEL5
STMSHOOT MERISTEMLESS
TALEthree-amino-acid-loop-extension
TFtranscription factor
WOXWUSCHEL-like HOMEOBOX

References

  1. Tsukaya, H. Leaf shape diversity with an emphasis on leaf contour variation, developmental background, and adaptation. Semin. Cell Dev. Biol. 2018, 79, 48–57. [Google Scholar] [CrossRef] [PubMed]
  2. Tsukaya, H. Leaf development. Arabidopsis Book/Am. Soc. Plant Biol. 2002, 1, e0072. [Google Scholar] [CrossRef] [PubMed]
  3. Du, F.; Guan, C.; Jiao, Y. Molecular mechanisms of leaf morphogenesis. Mol. Plant 2018, 11, 1117–1134. [Google Scholar] [CrossRef] [Green Version]
  4. Vogel, S. Leaves in the lowest and highest winds: Temperature, force and shape. New Phytol. 2009, 183, 13–26. [Google Scholar] [CrossRef] [PubMed]
  5. Nicotra, A.B.; Leigh, A.; Boyce, C.K.; Jones, C.S.; Niklas, K.J.; Royer, D.L.; Tsukaya, H. The evolution and functional significance of leaf shape in the angiosperms. Funct. Plant Biol. 2011, 38, 535–552. [Google Scholar] [CrossRef] [Green Version]
  6. Semchenko, M.; Zobel, K. The role of leaf lobation in elongation responses to shade in the rosette-forming forb Serratula tinctoria (Asteraceae). Ann. Bot. 2007, 100, 83–90. [Google Scholar] [CrossRef] [Green Version]
  7. Sisó, S.; Camarero, J.; Gil-Pelegrín, E. Relationship between hydraulic resistance and leaf morphology in broadleaf Quercus species: A new interpretation of leaf lobation. Trees 2001, 15, 341–345. [Google Scholar] [CrossRef]
  8. Tsukaya, H. Leaf shape: Genetic controls and environmental factors. Int. J. Dev. Biol. 2004, 49, 547–555. [Google Scholar] [CrossRef] [Green Version]
  9. Farquharson, K.L. Examining the molecular basis of heterophylly in North American lake cress. Plant Cell 2014, 26, 4567. [Google Scholar] [CrossRef] [Green Version]
  10. Nakayama, H.; Nakayama, N.; Seiki, S.; Kojima, M.; Sakakibara, H.; Sinha, N.; Kimura, S. Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American lake cress. Plant Cell 2014, 26, 4733–4748. [Google Scholar] [CrossRef]
  11. Niu, X.; Fu, D. The Roles of BLH Transcription Factors in Plant Development and Environmental Response. Int. J. Mol. Sci. 2022, 23, 3731. [Google Scholar] [CrossRef]
  12. Rast-Somssich, M.I.; Broholm, S.; Jenkins, H.; Canales, C.; Vlad, D.; Kwantes, M.; Bilsborough, G.; Ioio, R.D.; Ewing, R.M.; Laufs, P. Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta. Genes Dev. 2015, 29, 2391–2404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Vlad, D.; Kierzkowski, D.; Rast, M.I.; Vuolo, F.; Ioio, R.D.; Galinha, C.; Gan, X.; Hajheidari, M.; Hay, A.; Smith, R.S. Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 2014, 343, 780–783. [Google Scholar] [CrossRef] [PubMed]
  14. Ha, C.M.; Jun, J.H.; Fletcher, J.C. Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics 2010, 186, 197–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Vuolo, F.; Kierzkowski, D.; Runions, A.; Hajheidari, M.; Mentink, R.A.; Gupta, M.D.; Zhang, Z.; Vlad, D.; Wang, Y.; Pecinka, A. LMI1 homeodomain protein regulates organ proportions by spatial modulation of endoreduplication. Genes Dev. 2018, 32, 1361–1366. [Google Scholar] [CrossRef] [Green Version]
  16. Hasson, A.; Plessis, A.; Blein, T.; Adroher, B.; Grigg, S.; Tsiantis, M.; Boudaoud, A.; Damerval, C.; Laufs, P. Evolution and diverse roles of the CUP-SHAPED COTYLEDON genes in Arabidopsis leaf development. Plant Cell 2011, 23, 54–68. [Google Scholar] [CrossRef] [Green Version]
  17. Jiao, K.; Li, X.; Guo, Y.; Guan, Y.; Guo, W.; Luo, D.; Hu, Z.; Shen, Z. Regulation of compound leaf development in mungbean (Vigna radiata L.) by CUP-SHAPED COTYLEDON/NO APICAL MERISTEM (CUC/NAM) gene. Planta 2019, 249, 765–774. [Google Scholar] [CrossRef]
  18. Bharathan, G.; Goliber, T.E.; Moore, C.; Kessler, S.; Pham, T.; Sinha, N.R. Homologies in leaf form inferred from KNOXI gene expression during development. Science 2002, 296, 1858–1860. [Google Scholar] [CrossRef]
  19. Hareven, D.; Gutfinger, T.; Parnis, A.; Eshed, Y.; Lifschitz, E. The making of a compound leaf: Genetic manipulation of leaf architecture in tomato. Cell 1996, 84, 735–744. [Google Scholar] [CrossRef] [Green Version]
  20. Hay, A.; Tsiantis, M. KNOX genes: Versatile regulators of plant development and diversity. Development 2010, 137, 3153–3165. [Google Scholar] [CrossRef]
  21. Vuolo, F.; Mentink, R.A.; Hajheidari, M.; Bailey, C.D.; Filatov, D.A.; Tsiantis, M. Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity. Genes Dev. 2016, 30, 2370–2375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Kierzkowski, D.; Runions, A.; Vuolo, F.; Strauss, S.; Lymbouridou, R.; Routier-Kierzkowska, A.L.; Wilson-Sánchez, D.; Jenke, H.; Galinha, C.; Mosca, G.; et al. A Growth-Based Framework for Leaf Shape Development and Diversity. Cell 2019, 177, 1405–1418.e17. [Google Scholar] [CrossRef] [PubMed]
  23. Shani, E.; Ben-Gera, H.; Shleizer-Burko, S.; Burko, Y.; Weiss, D.; Ori, N. Cytokinin regulates compound leaf development in tomato. Plant Cell 2010, 22, 3206–3217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Streubel, S.; Fritz, M.A.; Teltow, M.; Kappel, C.; Sicard, A. Successive duplication-divergence mechanisms at the RCO locus contributed to leaf shape diversity in the Brassicaceae. Development 2018, 145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Ichihashi, Y.; Aguilar-Martínez, J.A.; Farhi, M.; Chitwood, D.H.; Kumar, R.; Millon, L.V.; Peng, J.; Maloof, J.N.; Sinha, N.R. Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape. Proc. Natl. Acad. Sci. USA 2014, 111, E2616–E2621. [Google Scholar] [CrossRef] [Green Version]
  26. Scanlon, M.J. The polar auxin transport inhibitor N-1-naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol. 2003, 133, 597–605. [Google Scholar] [CrossRef] [Green Version]
  27. Jasinski, S.; Piazza, P.; Craft, J.; Hay, A.; Woolley, L.; Rieu, I.; Phillips, A.; Hedden, P.; Tsiantis, M. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 2005, 15, 1560–1565. [Google Scholar] [CrossRef] [Green Version]
  28. Li, Z.; Li, B.; Liu, J.; Guo, Z.; Liu, Y.; Li, Y.; Shen, W.H.; Huang, Y.; Huang, H.; Zhang, Y. Transcription factors AS1 and AS2 interact with LHP1 to repress KNOX genes in Arabidopsis. J. Integr. Plant Biol. 2016, 58, 959–970. [Google Scholar] [CrossRef] [Green Version]
  29. Hay, A.; Barkoulas, M.; Tsiantis, M. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 2006, 133, 3955–3961. [Google Scholar] [CrossRef] [Green Version]
  30. Spinelli, S.V.; Martin, A.P.; Viola, I.L.; Gonzalez, D.H.; Palatnik, J.F. A mechanistic link between STM and CUC1 during Arabidopsis development. Plant Physiol. 2011, 156, 1894–1904. [Google Scholar] [CrossRef]
  31. Pulido, A.; Laufs, P. Co-ordination of developmental processes by small RNAs during leaf development. J. Exp. Bot. 2010, 61, 1277–1291. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Kawamura, E.; Horiguchi, G.; Tsukaya, H. Mechanisms of leaf tooth formation in Arabidopsis. Plant J. 2010, 62, 429–441. [Google Scholar] [CrossRef] [PubMed]
  33. Smith, L.G.; Hake, S. The initiation and determination of leaves. Plant Cell 1992, 4, 1017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Fletcher, J.C. The CLV-WUS Stem Cell Signaling Pathway: A Roadmap to Crop Yield Optimization. Plants 2018, 7, 87. [Google Scholar] [CrossRef] [Green Version]
  35. Kessler, S.; Sinha, N. Shaping up: The genetic control of leaf shape. Curr. Opin. Plant Biol. 2004, 7, 65–72. [Google Scholar] [CrossRef]
  36. Steeves, T.A.; Sussex, I.M. Patterns in Plant Development; Cambridge University Press: Cambridge, UK, 1989. [Google Scholar]
  37. Byrne, M.E. Making leaves. Curr. Opin. Plant Biol. 2012, 15, 24–30. [Google Scholar] [CrossRef]
  38. Shwartz, I.; Levy, M.; Ori, N.; Bar, M. Hormones in tomato leaf development. Dev. Biol. 2016, 419, 132–142. [Google Scholar] [CrossRef]
  39. Whitewoods, C.D.; Gonçalves, B.; Cheng, J.; Cui, M.; Kennaway, R.; Lee, K.; Bushell, C.; Yu, M.; Piao, C.; Coen, E. Evolution of carnivorous traps from planar leaves through simple shifts in gene expression. Science 2020, 367, 91–96. [Google Scholar] [CrossRef]
  40. Floyd, S.K.; Bowman, J.L. Gene expression patterns in seed plant shoot meristems and leaves: Homoplasy or homology? J. Plant Res. 2010, 123, 43–55. [Google Scholar] [CrossRef]
  41. Donnelly, P.M.; Bonetta, D.; Tsukaya, H.; Dengler, R.E.; Dengler, N.G. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 1999, 215, 407–419. [Google Scholar] [CrossRef]
  42. Endrizzi, K.; Moussian, B.; Haecker, A.; Levin, J.Z.; Laux, T. The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J. 1996, 10, 967–979. [Google Scholar] [CrossRef] [PubMed]
  43. Traas, J. Organogenesis at the Shoot Apical Meristem. Plants 2019, 8, 6. [Google Scholar] [CrossRef] [Green Version]
  44. Di Giacomo, E.; Iannelli, M.; Frugis, G. TALE and shape: How to make a leaf different. Plants 2013, 2, 317–342. [Google Scholar] [CrossRef] [Green Version]
  45. Shani, E.; Burko, Y.; Ben-Yaakov, L.; Berger, Y.; Amsellem, Z.; Goldshmidt, A.; Sharon, E.; Ori, N. Stage-specific regulation of Solanum lycopersicum leaf maturation by class 1 KNOTTED1-LIKE HOMEOBOX proteins. Plant Cell 2009, 21, 3078–3092. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Long, J.A.; Moan, E.I.; Medford, J.I.; Barton, M.K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 1996, 379, 66. [Google Scholar] [CrossRef]
  47. Lenhard, M.; Jürgens, G.; Laux, T. The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 2002, 129, 3195–3206. [Google Scholar] [CrossRef] [PubMed]
  48. Heisler, M.G.; Ohno, C.; Das, P.; Sieber, P.; Reddy, G.V.; Long, J.A.; Meyerowitz, E.M. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 2005, 15, 1899–1911. [Google Scholar] [CrossRef] [Green Version]
  49. Barton, M.K.; Poethig, R.S. Formation of the shoot apical meristem in Arabidopsis thaliana: An analysis of development in the wild type and in the shoot meristemless mutant. Development 1993, 119, 823–831. [Google Scholar] [CrossRef]
  50. Clark, S.E.; Jacobsen, S.E.; Levin, J.Z.; Meyerowitz, E.M. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 1996, 122, 1567–1575. [Google Scholar] [CrossRef]
  51. Chuck, G.; Lincoln, C.; Hake, S. KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 1996, 8, 1277–1289. [Google Scholar]
  52. Sentoku, N.; Sato, Y.; Matsuoka, M. Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice plants. Dev. Biol. 2000, 220, 358–364. [Google Scholar] [CrossRef] [PubMed]
  53. Kerstetter, R.; Vollbrecht, E.; Lowe, B.; Veit, B.; Yamaguchi, J.; Hake, S. Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 1994, 6, 1877–1887. [Google Scholar] [PubMed] [Green Version]
  54. Vollbrecht, E.; Veit, B.; Sinha, N.; Hake, S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 1991, 350, 241. [Google Scholar] [CrossRef] [PubMed]
  55. Mukherjee, K.; Brocchieri, L.; Bürglin, T.R. A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol. Biol. Evol. 2009, 26, 2775–2794. [Google Scholar] [CrossRef] [Green Version]
  56. Freeling, M.; Hake, S. Developmental genetics of mutants that specify knotted leaves in maize. Genetics 1985, 111, 617–634. [Google Scholar] [CrossRef]
  57. Furumizu, C.; Alvarez, J.P.; Sakakibara, K.; Bowman, J.L. Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication. PLoS Genet. 2015, 11, e1004980. [Google Scholar] [CrossRef] [Green Version]
  58. Hake, S.; Smith, H.M.; Holtan, H.; Magnani, E.; Mele, G.; Ramirez, J. The role of knox genes in plant development. Annu. Rev. Cell Dev. Biol. 2004, 20, 125–151. [Google Scholar] [CrossRef]
  59. Serikawa, K.A.; Martinez-Laborda, A.; Kim, H.S.; Zambryski, P.C. Localization of expression of KNAT3, a class 2 knotted1-like gene. Plant J. 1997, 11, 853–861. [Google Scholar] [CrossRef]
  60. Chai, M.; Zhou, C.; Molina, I.; Fu, C.; Nakashima, J.; Li, G.; Zhang, W.; Park, J.; Tang, Y.; Jiang, Q.; et al. A class II KNOX gene, KNOX4, controls seed physical dormancy. Proc. Natl. Acad. Sci. USA 2016, 113, 6997–7002. [Google Scholar] [CrossRef] [Green Version]
  61. Wang, S.; Yamaguchi, M.; Grienenberger, E.; Martone, P.T.; Samuels, A.L.; Mansfield, S.D. The Class II KNOX genes KNAT3 and KNAT7 work cooperatively to influence deposition of secondary cell walls that provide mechanical support to Arabidopsis stems. Plant J. 2020, 101, 293–309. [Google Scholar] [CrossRef]
  62. Byrne, M.E.; Barley, R.; Curtis, M.; Arroyo, J.M.; Dunham, M.; Hudson, A.; Martienssen, R.A. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 2000, 408, 967. [Google Scholar] [CrossRef] [PubMed]
  63. Ori, N.; Eshed, Y.; Chuck, G.; Bowman, J.L.; Hake, S. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 2000, 127, 5523–5532. [Google Scholar] [CrossRef] [PubMed]
  64. Semiarti, E.; Ueno, Y.; Tsukaya, H.; Iwakawa, H.; Machida, C.; Machida, Y. The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 2001, 128, 1771–1783. [Google Scholar] [CrossRef]
  65. Tsukaya, H.; Uchimiya, H. Genetic analyses of the formation of the serrated margin of leaf blades in Arabidopsis: Combination of a mutational analysis of leaf morphogenesis with the characterization of a specific marker gene expressed in hydathodes and stipules. Mol. Gen. Genet. MGG 1997, 256, 231–238. [Google Scholar] [CrossRef] [PubMed]
  66. Byrne, M.E.; Simorowski, J.; Martienssen, R.A. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 2002, 129, 1957–1965. [Google Scholar] [CrossRef]
  67. Ikezaki, M.; Kojima, M.; Sakakibara, H.; Kojima, S.; Ueno, Y.; Machida, C.; Machida, Y. Genetic networks regulated by ASYMMETRIC LEAVES1 (AS1) and AS2 in leaf development in Arabidopsis thaliana: KNOX genes control five morphological events. Plant J. 2010, 61, 70–82. [Google Scholar] [CrossRef]
  68. Guo, M.; Thomas, J.; Collins, G.; Timmermans, M.C. Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 2008, 20, 48–58. [Google Scholar] [CrossRef] [Green Version]
  69. Ha, C.M.; Jun, J.H.; Nam, H.G.; Fletcher, J.C. BLADE-ON-PETIOLE1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 2007, 19, 1809–1825. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Ha, C.M.; Kim, G.-T.; Kim, B.C.; Jun, J.H.; Soh, M.S.; Ueno, Y.; Machida, Y.; Tsukaya, H.; Nam, H.G. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 2003, 130, 161–172. [Google Scholar] [CrossRef] [Green Version]
  71. Jun, J.H.; Ha, C.M.; Fletcher, J.C. BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in Arabidopsis by directly activating ASYMMETRIC LEAVES2. Plant Cell 2010, 22, 62–76. [Google Scholar] [CrossRef] [Green Version]
  72. Hay, A.; Kaur, H.; Phillips, A.; Hedden, P.; Hake, S.; Tsiantis, M. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 2002, 12, 1557–1565. [Google Scholar] [CrossRef]
  73. Sakamoto, T.; Kamiya, N.; Ueguchi-Tanaka, M.; Iwahori, S.; Matsuoka, M. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 2001, 15, 581–590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Kusaba, S.; Fukumoto, M.; Honda, C.; Yamaguchi, I.; Sakamoto, T.; Kano-Murakami, Y. Decreased GA1 Content Caused by the Overexpression ofOSH1 Is Accompanied by Suppression of GA 20-Oxidase Gene Expression. Plant Physiol. 1998, 117, 1179–1184. [Google Scholar] [CrossRef] [Green Version]
  75. Tanaka-Ueguchi, M.; Itoh, H.; Oyama, N.; Koshioka, M.; Matsuoka, M. Over-expression of a tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J. 1998, 15, 391–400. [Google Scholar] [CrossRef] [PubMed]
  76. Chen, H.; Banerjee, A.K.; Hannapel, D.J. The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J. 2004, 38, 276–284. [Google Scholar] [CrossRef]
  77. Bolduc, N.; Hake, S. The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 2009, 21, 1647–1658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Sakamoto, T.; Sakakibara, H.; Kojima, M.; Yamamoto, Y.; Nagasaki, H.; Inukai, Y.; Sato, Y.; Matsuoka, M. Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol. 2006, 142, 54–62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Clouse, S.D.; Sasse, J.M. Brassinosteroids: Essential regulators of plant growth and development. Annu. Rev. Plant Biol. 1998, 49, 427–451. [Google Scholar] [CrossRef] [Green Version]
  80. Sun, Y.; Fan, X.-Y.; Cao, D.-M.; Tang, W.; He, K.; Zhu, J.-Y.; He, J.-X.; Bai, M.-Y.; Zhu, S.; Oh, E. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 2010, 19, 765–777. [Google Scholar] [CrossRef] [Green Version]
  81. Song, X.; Qi, Z.; Ahammed, G.J.; Yu, J.; Xia, X. Chapter 3—Brassinosteroids’ regulation of plant architecture. In Brassinosteroids in Plant Developmental Biology and Stress Tolerance; Ahammed, G.J., Sharma, A., Yu, J., Eds.; Academic Press: Cambridge, MA, USA, 2022; pp. 43–57. [Google Scholar]
  82. Gendron, J.M.; Liu, J.S.; Fan, M.; Bai, M.Y.; Wenkel, S.; Springer, P.S.; Barton, M.K.; Wang, Z.Y. Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc. Natl. Acad. Sci. USA 2012, 109, 21152–21157. [Google Scholar] [CrossRef] [Green Version]
  83. Tsuda, K.; Kurata, N.; Ohyanagi, H.; Hake, S. Genome-wide study of KNOX regulatory network reveals brassinosteroid catabolic genes important for shoot meristem function in rice. Plant Cell 2014, 26, 3488–3500. [Google Scholar] [CrossRef] [PubMed]
  84. Sakamoto, T.; Kawabe, A.; Tokida-Segawa, A.; Shimizu, B.i.; Takatsuto, S.; Shimada, Y.; Fujioka, S.; Mizutani, M. Rice CYP734As function as multisubstrate and multifunctional enzymes in brassinosteroid catabolism. Plant J. 2011, 67, 1–12. [Google Scholar] [CrossRef] [PubMed]
  85. Farquharson, K.L. A Rice KNOX Transcription Factor Represses Brassinosteroid Production in the Shoot Apical Meristem. Am. Soc. Plant Biol. 2014, 26, 3496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Scarpella, E.; Barkoulas, M.; Tsiantis, M. Control of leaf and vein development by auxin. Cold Spring Harb. Perspect Biol. 2010, 2, a001511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  87. Qi, J.; Wang, Y.; Yu, T.; Cunha, A.; Wu, B.; Vernoux, T.; Meyerowitz, E.; Jiao, Y. Auxin depletion from leaf primordia contributes to organ patterning. Proc. Natl. Acad. Sci. USA 2014, 111, 18769–18774. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  88. Ljung, K.; Bhalerao, R.P.; Sandberg, G. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J. 2001, 28, 465–474. [Google Scholar] [CrossRef]
  89. Zhang, Z.; Runions, A.; Mentink, R.A.; Kierzkowski, D.; Karady, M.; Hashemi, B.; Huijser, P.; Strauss, S.; Gan, X.; Ljung, K.; et al. A WOX/Auxin Biosynthesis Module Controls Growth to Shape Leaf Form. Curr. Biol. 2020, 30, 4857–4868.e6. [Google Scholar] [CrossRef]
  90. Aida, M.; Ishida, T.; Fukaki, H.; Fujisawa, H.; Tasaka, M. Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 1997, 9, 841–857. [Google Scholar] [CrossRef] [Green Version]
  91. Long, J.A.; Barton, M.K. The development of apical embryonic pattern in Arabidopsis. Development 1998, 125, 3027–3035. [Google Scholar] [CrossRef]
  92. Vroemen, C.W.; Mordhorst, A.P.; Albrecht, C.; Kwaaitaal, M.A.; de Vries, S.C. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 2003, 15, 1563–1577. [Google Scholar] [CrossRef]
  93. Aida, M.; Ishida, T.; Tasaka, M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: Interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 1999, 126, 1563–1570. [Google Scholar] [CrossRef] [PubMed]
  94. Somssich, M.; Je, B.I.; Simon, R.; Jackson, D. CLAVATA-WUSCHEL signaling in the shoot meristem. Development 2016, 143, 3238–3248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Yadav, R.K.; Perales, M.; Gruel, J.; Girke, T.; Jönsson, H.; Reddy, G.V. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 2011, 25, 2025–2030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Lopes, F.L.; Galvan-Ampudia, C.; Landrein, B. WUSCHEL in the shoot apical meristem: Old player, new tricks. J. Exp. Bot. 2020, 72, 1527–1535. [Google Scholar] [CrossRef]
  97. Su, Y.H.; Zhou, C.; Li, Y.J.; Yu, Y.; Tang, L.P.; Zhang, W.J.; Yao, W.J.; Huang, R.; Laux, T.; Zhang, X.S. Integration of pluripotency pathways regulates stem cell maintenance in the shoot meristem. Proc. Natl. Acad. Sci. USA 2020, 117, 22561–22571. [Google Scholar] [CrossRef]
  98. Felipo-Benavent, A.; Úrbez, C.; Blanco-Touriñán, N.; Serrano-Mislata, A.; Baumberger, N.; Achard, P.; Agustí, J.; Blázquez, M.A.; Alabadí, D. Regulation of xylem fiber differentiation by gibberellins through DELLA-KNAT1 interaction. Development 2018, 145. [Google Scholar] [CrossRef] [Green Version]
  99. Emery, J.F.; Floyd, S.K.; Alvarez, J.; Eshed, Y.; Hawker, N.P.; Izhaki, A.; Baum, S.F.; Bowman, J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 2003, 13, 1768–1774. [Google Scholar] [CrossRef] [Green Version]
  100. McConnell, J.R.; Emery, J.; Eshed, Y.; Bao, N.; Bowman, J.; Barton, M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411, 709. [Google Scholar] [CrossRef]
  101. Tatematsu, K.; Toyokura, K.; Miyashima, S.; Nakajima, K.; Okada, K. A molecular mechanism that confines the activity pattern of miR165 in Arabidopsis leaf primordia. Plant J. 2015, 82, 596–608. [Google Scholar] [CrossRef]
  102. Jia, X.; Ding, N.; Fan, W.; Yan, J.; Gu, Y.; Tang, X.; Li, R.; Tang, G. Functional plasticity of miR165/166 in plant development revealed by small tandem target mimic. Plant Sci. 2015, 233, 11–21. [Google Scholar] [CrossRef]
  103. Merelo, P.; Ram, H.; Caggiano, M.P.; Ohno, C.; Ott, F.; Straub, D.; Graeff, M.; Cho, S.K.; Yang, S.W.; Wenkel, S. Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity. Proc. Natl. Acad. Sci. USA 2016, 113, 11973–11978. [Google Scholar] [CrossRef] [PubMed]
  104. Kerstetter, R.A.; Bollman, K.; Taylor, R.A.; Bomblies, K.; Poethig, R.S. KANADI regulates organ polarity in Arabidopsis. Nature 2001, 411, 706. [Google Scholar] [CrossRef] [PubMed]
  105. Chen, X.; Wang, H.; Li, J.; Huang, H.; Xu, L. Quantitative control of ASYMMETRIC LEAVES2 expression is critical for leaf axial patterning in Arabidopsis. J. Exp. Bot. 2013, 64, 4895–4905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  106. Adams, W.W.; Terashima, I. The Leaf: A Platform for Performing Photosynthesis; Springer: Berlin, Germany, 2018; Volume 44. [Google Scholar]
  107. Canales, C.; Grigg, S.; Tsiantis, M. The formation and patterning of leaves: Recent advances. Planta 2005, 221, 752–756. [Google Scholar] [CrossRef]
  108. Pekker, I.; Alvarez, J.P.; Eshed, Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 2005, 17, 2899–2910. [Google Scholar] [CrossRef] [Green Version]
  109. Yamaguchi, T.; Nukazuka, A.; Tsukaya, H. Leaf adaxial–abaxial polarity specification and lamina outgrowth: Evolution and development. Plant Cell Physiol. 2012, 53, 1180–1194. [Google Scholar] [CrossRef]
  110. Garcia, D.; Collier, S.A.; Byrne, M.E.; Martienssen, R.A. Specification of Leaf Polarity in Arabidopsis via the trans-Acting siRNA Pathway. Curr. Biol. 2006, 16, 933–938. [Google Scholar] [CrossRef] [Green Version]
  111. Allen, E.; Xie, Z.; Gustafson, A.M.; Carrington, J.C. microRNA-Directed Phasing during Trans-Acting siRNA Biogenesis in Plants. Cell 2005, 121, 207–221. [Google Scholar] [CrossRef] [Green Version]
  112. Leigh, A.; Sevanto, S.; Close, J.D.; Nicotra, A.B. The influence of leaf size and shape on leaf thermal dynamics: Does theory hold up under natural conditions? Plant, Cell Environ. 2017, 40, 237–248. [Google Scholar] [CrossRef]
  113. Westoby, M.; Falster, D.S.; Moles, A.T.; Vesk, P.A.; Wright, I.J. Plant Ecological Strategies: Some Leading Dimensions of Variation Between Species. Annu. Rev. Ecol. Syst. 2002, 33, 125–159. [Google Scholar] [CrossRef] [Green Version]
  114. Lusk, C.H.; Grierson, E.R.P.; Laughlin, D.C. Large leaves in warm, moist environments confer an advantage in seedling light interception efficiency. New Phytol. 2019, 223, 1319–1327. [Google Scholar] [CrossRef] [PubMed]
  115. Baird, A.S.; Taylor, S.H.; Pasquet-Kok, J.; Vuong, C.; Zhang, Y.; Watcharamongkol, T.; Scoffoni, C.; Edwards, E.J.; Christin, P.-A.; Osborne, C.P.; et al. Developmental and biophysical determinants of grass leaf size worldwide. Nature 2021, 592, 242–247. [Google Scholar] [CrossRef] [PubMed]
  116. Barkoulas, M.; Galinha, C.; Grigg, S.P.; Tsiantis, M. From genes to shape: Regulatory interactions in leaf development. Curr. Opin. Plant Biol. 2007, 10, 660–666. [Google Scholar] [CrossRef]
  117. Powell, A.E.; Lenhard, M. Control of organ size in plants. Curr. Biol. 2012, 22, R360–R367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  118. Nath, U.; Crawford, B.C.; Carpenter, R.; Coen, E. Genetic control of surface curvature. Science 2003, 299, 1404–1407. [Google Scholar] [CrossRef] [Green Version]
  119. Palatnik, J.F.; Allen, E.; Wu, X.; Schommer, C.; Schwab, R.; Carrington, J.C.; Weigel, D. Control of leaf morphogenesis by microRNAs. Nature 2003, 425, 257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  120. Iwakawa, H.; Iwasaki, M.; Kojima, S.; Ueno, Y.; Soma, T.; Tanaka, H.; Semiarti, E.; Machida, Y.; Machida, C. Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. Plant J. 2007, 51, 173–184. [Google Scholar] [CrossRef] [PubMed]
  121. Waites, R.; Selvadurai, H.R.; Oliver, I.R.; Hudson, A. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 1998, 93, 779–789. [Google Scholar] [CrossRef] [Green Version]
  122. Tsiantis, M.; Schneeberger, R.; Golz, J.F.; Freeling, M.; Langdale, J.A. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 1999, 284, 154–156. [Google Scholar] [CrossRef] [Green Version]
  123. Iwakawa, H.; Ueno, Y.; Semiarti, E.; Onouchi, H.; Kojima, S.; Tsukaya, H.; Hasebe, M.; Soma, T.; Ikezaki, M.; Machida, C. The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 2002, 43, 467–478. [Google Scholar] [CrossRef] [Green Version]
  124. Zhou, C.; Han, L.; Li, G.; Chai, M.; Fu, C.; Cheng, X.; Wen, J.; Tang, Y.; Wang, Z.Y. STM/BP-Like KNOXI Is Uncoupled from ARP in the Regulation of Compound Leaf Development in Medicago truncatula. Plant Cell 2014, 26, 1464–1479. [Google Scholar] [CrossRef] [PubMed]
  125. Shi, J.; Dong, J.; Xue, J.; Wang, H.; Yang, Z.; Jiao, Y.; Xu, L.; Huang, H. Model for the role of auxin polar transport in patterning of the leaf adaxial–abaxial axis. Plant J. 2017, 92, 469–480. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  126. Challa, K.R.; Rath, M.; Sharma, A.N.; Bajpai, A.K.; Davuluri, S.; Acharya, K.K.; Nath, U. Active suppression of leaflet emergence as a mechanism of simple leaf development. Nat. Plants 2021, 7, 1264–1275. [Google Scholar] [CrossRef] [PubMed]
  127. Hay, A.; Tsiantis, M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 2006, 38, 942. [Google Scholar] [CrossRef]
  128. Souer, E.; van Houwelingen, A.; Kloos, D.; Mol, J.; Koes, R. The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 1996, 85, 159–170. [Google Scholar] [CrossRef] [Green Version]
  129. Aida, M.; Tasaka, M. Genetic control of shoot organ boundaries. Curr. Opin. Plant Biol. 2006, 9, 72–77. [Google Scholar] [CrossRef]
  130. Blein, T.; Pulido, A.; Vialette-Guiraud, A.; Nikovics, K.; Morin, H.; Hay, A.; Johansen, I.E.; Tsiantis, M.; Laufs, P. A conserved molecular framework for compound leaf development. Science 2008, 322, 1835–1839. [Google Scholar] [CrossRef] [Green Version]
  131. Bilsborough, G.D.; Runions, A.; Barkoulas, M.; Jenkins, H.W.; Hasson, A.; Galinha, C.; Laufs, P.; Hay, A.; Prusinkiewicz, P.; Tsiantis, M. Model for the regulation of Arabidopsis thaliana leaf margin development. Proc. Natl. Acad. Sci. USA 2011, 108, 3424–3429. [Google Scholar] [CrossRef] [Green Version]
  132. Nikovics, K.; Blein, T.; Peaucelle, A.; Ishida, T.; Morin, H.; Aida, M.; Laufs, P. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 2006, 18, 2929–2945. [Google Scholar] [CrossRef] [Green Version]
  133. Barkoulas, M.; Hay, A.; Kougioumoutzi, E.; Tsiantis, M. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat. Genet. 2008, 40, 1136. [Google Scholar] [CrossRef]
Forests 13 01726 g001 550
Figure 1. Interplay between genes in the shoot apical meristem (SAM) and leaf primordium (LP): (a) the regulation of SAM maintenance and organogenesis; (b) the genetic regulatory networks of KNOXI; (c) the genetics interplay related to ad–ab polarity leaf establishment.
Figure 1. Interplay between genes in the shoot apical meristem (SAM) and leaf primordium (LP): (a) the regulation of SAM maintenance and organogenesis; (b) the genetic regulatory networks of KNOXI; (c) the genetics interplay related to ad–ab polarity leaf establishment.
Forests 13 01726 g001
Forests 13 01726 g002 550
Figure 2. Interplay of genes in determining leaf polarity and margin. The serrations at the leaf margin are contingent on the regulatory interplay of miR164–CUC–PIN–auxin. CUC genes facilitate the PIN-dependent generation of auxin maxima activity at the leaf margin. Conversely, miR164 represses the CUC gene, promoting smooth margin development.
Figure 2. Interplay of genes in determining leaf polarity and margin. The serrations at the leaf margin are contingent on the regulatory interplay of miR164–CUC–PIN–auxin. CUC genes facilitate the PIN-dependent generation of auxin maxima activity at the leaf margin. Conversely, miR164 represses the CUC gene, promoting smooth margin development.
Forests 13 01726 g002
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Ma, J.; Li, H. The Formation of Shapes: Interplay of Genes during Leaf Development Processes. Forests 2022, 13, 1726. https://doi.org/10.3390/f13101726

AMA Style

Ma J, Li H. The Formation of Shapes: Interplay of Genes during Leaf Development Processes. Forests. 2022; 13(10):1726. https://doi.org/10.3390/f13101726

Chicago/Turabian Style

Ma, Jikai, and Huogen Li. 2022. "The Formation of Shapes: Interplay of Genes during Leaf Development Processes" Forests 13, no. 10: 1726. https://doi.org/10.3390/f13101726

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop