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Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth.

Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T - PLoS Genet. (2011)

Bottom Line: Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity.Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments.By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation.

View Article: PubMed Central - PubMed

Affiliation: Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna, Austria.

ABSTRACT
Cell-to-cell communication is crucial for the development of multicellular organisms, especially during the generation of new tissues and organs. Secondary growth--the lateral expansion of plant growth axes--is a highly dynamic process that depends on the activity of the cambium. The cambium is a stem cell-like tissue whose activity is responsible for wood production and, thus, for the establishment of extended shoot and root systems. Attempts to study cambium regulation at the molecular level have been hampered by the limitations of performing genetic analyses in trees and by the difficulty of accessing this tissue in model systems such as Arabidopsis thaliana. Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity. Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments. By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation. In summary, we provide a means for investigating cambium regulation in unprecedented depth and present two signaling components that control a process responsible for the accumulation of a large proportion of terrestrial biomass.

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In vitro-induction of secondary growth (CIS–incubation).(A and B) Comparison of cross-sections from a primary (A) and secondary (B) stem (IC: arrows in B). Blue: xylem/xylem fibers; red: fascicular and interfascicular cambium; yellow: phloem/phloem parenchyma; green: starch sheath. Triangle: see Figure 2H. (C) Origin of stem fragments for CIS-incubation. At the stage of collection, IC initiation was restricted to the region labeled in red [4]. (D) Experimental setup of CIS. (E–G) Stem fragments incubated without (E) and with (F) apically applied NAA in comparison to a stem immediately above the uppermost rosette leaf of a 15 cm tall plant (G). Arrows indicate dividing tissues in interfascicular regions. (H and I). Fragments incubated with basally applied NAA (H) and with apically applied NAA together with ubiquitously applied NPA (I, 1 µg/ml). Size bar in (E): 100 µm, same magnification in (E–I). The positions of primary vascular bundles are labeled by asterisks.
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pgen-1001312-g001: In vitro-induction of secondary growth (CIS–incubation).(A and B) Comparison of cross-sections from a primary (A) and secondary (B) stem (IC: arrows in B). Blue: xylem/xylem fibers; red: fascicular and interfascicular cambium; yellow: phloem/phloem parenchyma; green: starch sheath. Triangle: see Figure 2H. (C) Origin of stem fragments for CIS-incubation. At the stage of collection, IC initiation was restricted to the region labeled in red [4]. (D) Experimental setup of CIS. (E–G) Stem fragments incubated without (E) and with (F) apically applied NAA in comparison to a stem immediately above the uppermost rosette leaf of a 15 cm tall plant (G). Arrows indicate dividing tissues in interfascicular regions. (H and I). Fragments incubated with basally applied NAA (H) and with apically applied NAA together with ubiquitously applied NPA (I, 1 µg/ml). Size bar in (E): 100 µm, same magnification in (E–I). The positions of primary vascular bundles are labeled by asterisks.

Mentions: The development of multicellular organisms requires extensive cell-to-cell communication to integrate the activity of single cells into the context of the whole organism. Plant development is especially demanding in this respect due to the high degree of plasticity caused by their interdependence with external cues. The capacity to establish pluripotent and proliferating tissues - the meristems - from differentiated cells represents a remarkable example of this developmental plasticity, which has been the focus of extensive research in the past [1]–[3]. The formation of the interfascicular cambium (Figure 1A, 1B) is one of the few instances in which post-embryonic de novo-initiation of meristematic activity occurs during normal plant development [4], and thus serves as an attractive model for studying the complexity of cell fate regulation in general, and cambium regulation in particular.


Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth.

Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T - PLoS Genet. (2011)

In vitro-induction of secondary growth (CIS–incubation).(A and B) Comparison of cross-sections from a primary (A) and secondary (B) stem (IC: arrows in B). Blue: xylem/xylem fibers; red: fascicular and interfascicular cambium; yellow: phloem/phloem parenchyma; green: starch sheath. Triangle: see Figure 2H. (C) Origin of stem fragments for CIS-incubation. At the stage of collection, IC initiation was restricted to the region labeled in red [4]. (D) Experimental setup of CIS. (E–G) Stem fragments incubated without (E) and with (F) apically applied NAA in comparison to a stem immediately above the uppermost rosette leaf of a 15 cm tall plant (G). Arrows indicate dividing tissues in interfascicular regions. (H and I). Fragments incubated with basally applied NAA (H) and with apically applied NAA together with ubiquitously applied NPA (I, 1 µg/ml). Size bar in (E): 100 µm, same magnification in (E–I). The positions of primary vascular bundles are labeled by asterisks.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3040665&req=5

pgen-1001312-g001: In vitro-induction of secondary growth (CIS–incubation).(A and B) Comparison of cross-sections from a primary (A) and secondary (B) stem (IC: arrows in B). Blue: xylem/xylem fibers; red: fascicular and interfascicular cambium; yellow: phloem/phloem parenchyma; green: starch sheath. Triangle: see Figure 2H. (C) Origin of stem fragments for CIS-incubation. At the stage of collection, IC initiation was restricted to the region labeled in red [4]. (D) Experimental setup of CIS. (E–G) Stem fragments incubated without (E) and with (F) apically applied NAA in comparison to a stem immediately above the uppermost rosette leaf of a 15 cm tall plant (G). Arrows indicate dividing tissues in interfascicular regions. (H and I). Fragments incubated with basally applied NAA (H) and with apically applied NAA together with ubiquitously applied NPA (I, 1 µg/ml). Size bar in (E): 100 µm, same magnification in (E–I). The positions of primary vascular bundles are labeled by asterisks.
Mentions: The development of multicellular organisms requires extensive cell-to-cell communication to integrate the activity of single cells into the context of the whole organism. Plant development is especially demanding in this respect due to the high degree of plasticity caused by their interdependence with external cues. The capacity to establish pluripotent and proliferating tissues - the meristems - from differentiated cells represents a remarkable example of this developmental plasticity, which has been the focus of extensive research in the past [1]–[3]. The formation of the interfascicular cambium (Figure 1A, 1B) is one of the few instances in which post-embryonic de novo-initiation of meristematic activity occurs during normal plant development [4], and thus serves as an attractive model for studying the complexity of cell fate regulation in general, and cambium regulation in particular.

Bottom Line: Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity.Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments.By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation.

View Article: PubMed Central - PubMed

Affiliation: Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna, Austria.

ABSTRACT
Cell-to-cell communication is crucial for the development of multicellular organisms, especially during the generation of new tissues and organs. Secondary growth--the lateral expansion of plant growth axes--is a highly dynamic process that depends on the activity of the cambium. The cambium is a stem cell-like tissue whose activity is responsible for wood production and, thus, for the establishment of extended shoot and root systems. Attempts to study cambium regulation at the molecular level have been hampered by the limitations of performing genetic analyses in trees and by the difficulty of accessing this tissue in model systems such as Arabidopsis thaliana. Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity. Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments. By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation. In summary, we provide a means for investigating cambium regulation in unprecedented depth and present two signaling components that control a process responsible for the accumulation of a large proportion of terrestrial biomass.

Show MeSH
Related in: MedlinePlus