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Behavior of Leaf Meristems and Their Modification.

Ichihashi Y, Tsukaya H - Front Plant Sci (2015)

Bottom Line: Leaf organogenesis depends on activities of several distinct meristems that are established and spatiotemporally differentiated after the initiation of leaf primordia.Here, we review recent findings in the gene regulatory networks that orchestrate leaf meristem activities in a model plant Arabidopsis thaliana.We then discuss recent key studies investigating the natural variation in leaf morphology to understand how the gene regulatory networks modulate leaf meristems to yield a substantial diversity of leaf forms during the course of evolution.

View Article: PubMed Central - PubMed

Affiliation: RIKEN Center for Sustainable Resource Science Yokohama, Japan.

ABSTRACT
A major source of diversity in flowering plant form is the extensive variability of leaf shape and size. Leaf formation is initiated by recruitment of a handful of cells flanking the shoot apical meristem (SAM) to develop into a complex three-dimensional structure. Leaf organogenesis depends on activities of several distinct meristems that are established and spatiotemporally differentiated after the initiation of leaf primordia. Here, we review recent findings in the gene regulatory networks that orchestrate leaf meristem activities in a model plant Arabidopsis thaliana. We then discuss recent key studies investigating the natural variation in leaf morphology to understand how the gene regulatory networks modulate leaf meristems to yield a substantial diversity of leaf forms during the course of evolution.

No MeSH data available.


Related in: MedlinePlus

Gene regulatory networks of leaf development. (A) Regulators of leaf structural identification and leaf cell proliferation in Arabidopsis thaliana. Arrows, T bars, and lines indicate positive regulation, negative regulation, and protein-protein interactions, respectively. (B) Schematic diagram representing the gene regulatory networks controlling tomato leaf development, which consists of several peripheral gene network modules and a core network having highly interconnected genes. KNOX appears as a bottleneck in the network, suggesting that KNOX was an evolutionary hot spot that was repeatedly recruited for generating natural variation in leaf shape. KNOX regulation occurs at multiple levels including (1) modulation of trans-acting factors regulating KNOX (Ichihashi et al., 2014), (2) promoter changes at KNOX (Piazza et al., 2010), (3) changes in KNOX expression patterns (Bharathan et al., 2002), and (4) changes in effective KNOX protein concentration (Kimura et al., 2008).
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Figure 2: Gene regulatory networks of leaf development. (A) Regulators of leaf structural identification and leaf cell proliferation in Arabidopsis thaliana. Arrows, T bars, and lines indicate positive regulation, negative regulation, and protein-protein interactions, respectively. (B) Schematic diagram representing the gene regulatory networks controlling tomato leaf development, which consists of several peripheral gene network modules and a core network having highly interconnected genes. KNOX appears as a bottleneck in the network, suggesting that KNOX was an evolutionary hot spot that was repeatedly recruited for generating natural variation in leaf shape. KNOX regulation occurs at multiple levels including (1) modulation of trans-acting factors regulating KNOX (Ichihashi et al., 2014), (2) promoter changes at KNOX (Piazza et al., 2010), (3) changes in KNOX expression patterns (Bharathan et al., 2002), and (4) changes in effective KNOX protein concentration (Kimura et al., 2008).

Mentions: A number of genes responsible for cell proliferation in leaf primordia have been identified in studies of A. thaliana mutants (Gonzalez et al., 2012; Kalve et al., 2014; Figure 2A). As previously mentioned, AN3 functions at the plate meristem to produce cells of both the leaf blade and the leaf petiole (Kim and Kende, 2004; Horiguchi et al., 2005; Ichihashi et al., 2011; Kawade et al., 2013). AN3 shows protein-protein interaction with GROWTHREGULATING FACTOR5 (GRF5) to promote cell proliferation (Horiguchi et al., 2005). AN3 is also known as GRF-INTERACTING FACTOR1 (GIF1), and other members of the GIF family, GIF2 and GIF3, also promote cell proliferation in a redundant fashion (Lee et al., 2009). AN3 binds to the SWITCH/SUCROSE NONFERMENTING (SWI/SNF) chromatin remodeling complexes to regulate transcription during leaf development (Vercruyssen et al., 2014). AN3 is also involved in the establishment of leaf identity in cotyledons via the repression of root fate during embryogenesis (Kanei et al., 2012). On the other hands KLU is expressed in the basal region of leaf primordia and generates a mobile growth factor (Anastasiou et al., 2007). PRS/WOX3 and WOX1 are also classified as activators of cell proliferation (Nakata et al., 2012). The auxin inducible gene AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE (ARGOS) increases the expression level of the D-type cyclin CYCD3;1 gene through the regulation of the AINTEGUMENTA genes (Krizek, 1999; Mizukami and Fischer, 2000; Hu et al., 2003; Nole-Wilson et al., 2005). APC10 and CDC27a are subunits of the anaphase-promoting complex/cyclosome (APC/C), which functions at the G2 to M transition of the cell cycle and is also reported to regulate leaf cell proliferation (Rojas et al., 2009; Eloy et al., 2011). In addition, the C2H2 zinc finger protein JAGGED (JAG) and a subunit of the Mediator complex STRUWWELPETER (SWP) are also constituent factors that positively control cell proliferation in leaves (Autran et al., 2002; Ohno et al., 2004). All of these genes function mainly in the control of lateral organ growth and not in the SAM and RAM. Therefore, a specialized set of genes is utilized to maintain leaf meristem activities.


Behavior of Leaf Meristems and Their Modification.

Ichihashi Y, Tsukaya H - Front Plant Sci (2015)

Gene regulatory networks of leaf development. (A) Regulators of leaf structural identification and leaf cell proliferation in Arabidopsis thaliana. Arrows, T bars, and lines indicate positive regulation, negative regulation, and protein-protein interactions, respectively. (B) Schematic diagram representing the gene regulatory networks controlling tomato leaf development, which consists of several peripheral gene network modules and a core network having highly interconnected genes. KNOX appears as a bottleneck in the network, suggesting that KNOX was an evolutionary hot spot that was repeatedly recruited for generating natural variation in leaf shape. KNOX regulation occurs at multiple levels including (1) modulation of trans-acting factors regulating KNOX (Ichihashi et al., 2014), (2) promoter changes at KNOX (Piazza et al., 2010), (3) changes in KNOX expression patterns (Bharathan et al., 2002), and (4) changes in effective KNOX protein concentration (Kimura et al., 2008).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664833&req=5

Figure 2: Gene regulatory networks of leaf development. (A) Regulators of leaf structural identification and leaf cell proliferation in Arabidopsis thaliana. Arrows, T bars, and lines indicate positive regulation, negative regulation, and protein-protein interactions, respectively. (B) Schematic diagram representing the gene regulatory networks controlling tomato leaf development, which consists of several peripheral gene network modules and a core network having highly interconnected genes. KNOX appears as a bottleneck in the network, suggesting that KNOX was an evolutionary hot spot that was repeatedly recruited for generating natural variation in leaf shape. KNOX regulation occurs at multiple levels including (1) modulation of trans-acting factors regulating KNOX (Ichihashi et al., 2014), (2) promoter changes at KNOX (Piazza et al., 2010), (3) changes in KNOX expression patterns (Bharathan et al., 2002), and (4) changes in effective KNOX protein concentration (Kimura et al., 2008).
Mentions: A number of genes responsible for cell proliferation in leaf primordia have been identified in studies of A. thaliana mutants (Gonzalez et al., 2012; Kalve et al., 2014; Figure 2A). As previously mentioned, AN3 functions at the plate meristem to produce cells of both the leaf blade and the leaf petiole (Kim and Kende, 2004; Horiguchi et al., 2005; Ichihashi et al., 2011; Kawade et al., 2013). AN3 shows protein-protein interaction with GROWTHREGULATING FACTOR5 (GRF5) to promote cell proliferation (Horiguchi et al., 2005). AN3 is also known as GRF-INTERACTING FACTOR1 (GIF1), and other members of the GIF family, GIF2 and GIF3, also promote cell proliferation in a redundant fashion (Lee et al., 2009). AN3 binds to the SWITCH/SUCROSE NONFERMENTING (SWI/SNF) chromatin remodeling complexes to regulate transcription during leaf development (Vercruyssen et al., 2014). AN3 is also involved in the establishment of leaf identity in cotyledons via the repression of root fate during embryogenesis (Kanei et al., 2012). On the other hands KLU is expressed in the basal region of leaf primordia and generates a mobile growth factor (Anastasiou et al., 2007). PRS/WOX3 and WOX1 are also classified as activators of cell proliferation (Nakata et al., 2012). The auxin inducible gene AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE (ARGOS) increases the expression level of the D-type cyclin CYCD3;1 gene through the regulation of the AINTEGUMENTA genes (Krizek, 1999; Mizukami and Fischer, 2000; Hu et al., 2003; Nole-Wilson et al., 2005). APC10 and CDC27a are subunits of the anaphase-promoting complex/cyclosome (APC/C), which functions at the G2 to M transition of the cell cycle and is also reported to regulate leaf cell proliferation (Rojas et al., 2009; Eloy et al., 2011). In addition, the C2H2 zinc finger protein JAGGED (JAG) and a subunit of the Mediator complex STRUWWELPETER (SWP) are also constituent factors that positively control cell proliferation in leaves (Autran et al., 2002; Ohno et al., 2004). All of these genes function mainly in the control of lateral organ growth and not in the SAM and RAM. Therefore, a specialized set of genes is utilized to maintain leaf meristem activities.

Bottom Line: Leaf organogenesis depends on activities of several distinct meristems that are established and spatiotemporally differentiated after the initiation of leaf primordia.Here, we review recent findings in the gene regulatory networks that orchestrate leaf meristem activities in a model plant Arabidopsis thaliana.We then discuss recent key studies investigating the natural variation in leaf morphology to understand how the gene regulatory networks modulate leaf meristems to yield a substantial diversity of leaf forms during the course of evolution.

View Article: PubMed Central - PubMed

Affiliation: RIKEN Center for Sustainable Resource Science Yokohama, Japan.

ABSTRACT
A major source of diversity in flowering plant form is the extensive variability of leaf shape and size. Leaf formation is initiated by recruitment of a handful of cells flanking the shoot apical meristem (SAM) to develop into a complex three-dimensional structure. Leaf organogenesis depends on activities of several distinct meristems that are established and spatiotemporally differentiated after the initiation of leaf primordia. Here, we review recent findings in the gene regulatory networks that orchestrate leaf meristem activities in a model plant Arabidopsis thaliana. We then discuss recent key studies investigating the natural variation in leaf morphology to understand how the gene regulatory networks modulate leaf meristems to yield a substantial diversity of leaf forms during the course of evolution.

No MeSH data available.


Related in: MedlinePlus