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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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Quantification of IC activity.(A–C) Lateral extension of the IC together with the IC-derived tissue (ICD) in different genetic backgrounds at different positions along the shoot base. See Figure S5 for allele characterization. Significance levels are indicated by asterisks with the corresponding color. (D–I) Histological representations of mol1-1 (D), rul1-2 (E), and pxy-4 (F) mutants in comparison to corresponding wild-type plants (G, H, I). Brackets indicate the extension of the ICD. (J–O) Higher magnification of mol1-1 (J), rul1-2 (H), pxy-4 (N) mutants and the corresponding wild-type plants (K, M, O) as shown in (D–I). Size bar in (D) and (J): 50 µm, same magnification in (D–I) and in (J–O). Sections from immediately above the uppermost rosette leaf are shown (i.e. position 0 in A–C). Positions of primary vascular bundles are labeled by asterisks in (E–I).
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pgen-1001312-g005: Quantification of IC activity.(A–C) Lateral extension of the IC together with the IC-derived tissue (ICD) in different genetic backgrounds at different positions along the shoot base. See Figure S5 for allele characterization. Significance levels are indicated by asterisks with the corresponding color. (D–I) Histological representations of mol1-1 (D), rul1-2 (E), and pxy-4 (F) mutants in comparison to corresponding wild-type plants (G, H, I). Brackets indicate the extension of the ICD. (J–O) Higher magnification of mol1-1 (J), rul1-2 (H), pxy-4 (N) mutants and the corresponding wild-type plants (K, M, O) as shown in (D–I). Size bar in (D) and (J): 50 µm, same magnification in (D–I) and in (J–O). Sections from immediately above the uppermost rosette leaf are shown (i.e. position 0 in A–C). Positions of primary vascular bundles are labeled by asterisks in (E–I).

Mentions: As IC initiation is a highly dynamic process likely to involve extensive cell-to-cell communication, we predicted that the identified signaling components play an important role in cambium regulation. To test this assumption, we analyzed lines impaired in the expression of the uncharacterized leucine-rich repeat receptor-like kinases (LRR-RLKs) present on our reduced list of genes (Table 1, Figure S5) and which we designated MORE LATERAL GROWTH1 (MOL1) and REDUCED IN LATERAL GROWTH1 (RUL1). As a reference for plants affected in cambium activity, we also included pxy-4 mutants [24] in our analysis. All homozygous T-DNA insertion lines (Figure S5) were indistinguishable from wild-type with respect to their overall growth behavior. Histological analyses showed that most pxy-4 mutant plants did not initiate IC formation (Figure 5), thus confirming the role of PXY in secondary growth and demonstrating that pxy-specific defects [26] prevent the establishment of a closed cambium cylinder in the stem. In contrast, IC was detected in the two other mutants with no sign of altered tissue patterning (Figure 5). However, mol1 mutants displayed an enhanced formation of secondary vascular tissue in fascicular and interfascicular regions that exceeded the wild-type by 30%, indicating a substantial increase in cambium activity. By contrast, IC-based tissue formation was decreased by 40% in rul1 mutants, suggesting a reduction in cambium activity in rul1 mutant backgrounds (Figure 5). These results indicate that both genes regulate the production of secondary vascular tissues with MOL1 functioning as a repressor, and RUL1 as an activator, of cambium activity.


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)

Quantification of IC activity.(A–C) Lateral extension of the IC together with the IC-derived tissue (ICD) in different genetic backgrounds at different positions along the shoot base. See Figure S5 for allele characterization. Significance levels are indicated by asterisks with the corresponding color. (D–I) Histological representations of mol1-1 (D), rul1-2 (E), and pxy-4 (F) mutants in comparison to corresponding wild-type plants (G, H, I). Brackets indicate the extension of the ICD. (J–O) Higher magnification of mol1-1 (J), rul1-2 (H), pxy-4 (N) mutants and the corresponding wild-type plants (K, M, O) as shown in (D–I). Size bar in (D) and (J): 50 µm, same magnification in (D–I) and in (J–O). Sections from immediately above the uppermost rosette leaf are shown (i.e. position 0 in A–C). Positions of primary vascular bundles are labeled by asterisks in (E–I).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3040665&req=5

pgen-1001312-g005: Quantification of IC activity.(A–C) Lateral extension of the IC together with the IC-derived tissue (ICD) in different genetic backgrounds at different positions along the shoot base. See Figure S5 for allele characterization. Significance levels are indicated by asterisks with the corresponding color. (D–I) Histological representations of mol1-1 (D), rul1-2 (E), and pxy-4 (F) mutants in comparison to corresponding wild-type plants (G, H, I). Brackets indicate the extension of the ICD. (J–O) Higher magnification of mol1-1 (J), rul1-2 (H), pxy-4 (N) mutants and the corresponding wild-type plants (K, M, O) as shown in (D–I). Size bar in (D) and (J): 50 µm, same magnification in (D–I) and in (J–O). Sections from immediately above the uppermost rosette leaf are shown (i.e. position 0 in A–C). Positions of primary vascular bundles are labeled by asterisks in (E–I).
Mentions: As IC initiation is a highly dynamic process likely to involve extensive cell-to-cell communication, we predicted that the identified signaling components play an important role in cambium regulation. To test this assumption, we analyzed lines impaired in the expression of the uncharacterized leucine-rich repeat receptor-like kinases (LRR-RLKs) present on our reduced list of genes (Table 1, Figure S5) and which we designated MORE LATERAL GROWTH1 (MOL1) and REDUCED IN LATERAL GROWTH1 (RUL1). As a reference for plants affected in cambium activity, we also included pxy-4 mutants [24] in our analysis. All homozygous T-DNA insertion lines (Figure S5) were indistinguishable from wild-type with respect to their overall growth behavior. Histological analyses showed that most pxy-4 mutant plants did not initiate IC formation (Figure 5), thus confirming the role of PXY in secondary growth and demonstrating that pxy-specific defects [26] prevent the establishment of a closed cambium cylinder in the stem. In contrast, IC was detected in the two other mutants with no sign of altered tissue patterning (Figure 5). However, mol1 mutants displayed an enhanced formation of secondary vascular tissue in fascicular and interfascicular regions that exceeded the wild-type by 30%, indicating a substantial increase in cambium activity. By contrast, IC-based tissue formation was decreased by 40% in rul1 mutants, suggesting a reduction in cambium activity in rul1 mutant backgrounds (Figure 5). These results indicate that both genes regulate the production of secondary vascular tissues with MOL1 functioning as a repressor, and RUL1 as an activator, of cambium activity.

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