A Local Maximum in Gibberellin Levels Regulates Maize Leaf Growth by Spatial Control of Cell Division

Nelissen, Hilde; Rymen, Bart; Demuynck, Kirin; Lijsebettens, Mieke Van; Kamiya, Yûji; Inzé, Dirk; Beemster, Gerrit T.S.

doi:10.1016/j.cub.2012.06.047

Cited by 74 publications

(158 citation statements)

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“…Our results are consistent with a role for RA1 in fine-tuning levels of bioactive GA 1 by direct binding and up-regulation of GA biosynthesis and catabolism genes, d1 (GA 3-oxidase 1, GRMZM2G036340) and ga2ox1, respectively. ga3-oxidase is rate-limiting and involved in spatiotemporal maintenance of GA 1 maxima during the developmental shift from cell division to differentiation (Nelissen et al 2012). Consistent with positive regulation of d1 by RA1, GA-responsive DELLA genes, d8 and d9, were significantly down-regulated in ra1 mutants.…”

Section: Network In Maize Inflorescence Developmentsupporting

confidence: 55%

Regulatory modules controlling maize inflorescence architecture

et al. 2013

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Genetic control of branching is a primary determinant of yield, regulating seed number and harvesting ability, yet little is known about the molecular networks that shape grain-bearing inflorescences of cereal crops. Here, we used the maize (Zea mays) inflorescence to investigate gene networks that modulate determinacy, specifically the decision to allow branch growth. We characterized developmental transitions by associating spatiotemporal expression profiles with morphological changes resulting from genetic perturbations that disrupt steps in a pathway controlling branching. Developmental dynamics of genes targeted in vivo by the transcription factor RAMOSA1, a key regulator of determinacy, revealed potential mechanisms for repressing branches in distinct stem cell populations, including interactions with KNOTTED1, a master regulator of stem cell maintenance. Our results uncover discrete developmental modules that function in determining grass-specific morphology and provide a basis for targeted crop improvement and translation to other cereal crops with comparable inflorescence architectures.

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Section: Network In Maize Inflorescence Developmentsupporting

confidence: 55%

Regulatory modules controlling maize inflorescence architecture

et al. 2013

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“…The expression of the maintenance DMT transcripts ZmMET (P = 1.3e-13), ZmCMT1 (P = 2.2e-16), and ZmCMT2 (P = 6.5e-14) follows more or less the same profile as that of ZmCDKB1;1 (P = 6.7e-8; Fig. 2B), encoding a CYCLIN-DEPENDENT KINASE and used here as a proxy for cell division (Rymen et al, 2007;Nelissen et al, 2012). The expression of ZmMET1 and ZmMET2 cannot be distinguished because of their high sequence similarity.…”

Section: Maize Maintenance Methyltransferases Are Highly Expressed Inmentioning

confidence: 82%

“…Combined with a kinematic analysis, this allows us to correlate the expression levels obtained by quantitative PCR to the cellular processes (Nelissen et al, 2012(Nelissen et al, , 2013. The expression of the maintenance DMT transcripts ZmMET (P = 1.3e-13), ZmCMT1 (P = 2.2e-16), and ZmCMT2 (P = 6.5e-14) follows more or less the same profile as that of ZmCDKB1;1 (P = 6.7e-8; Fig.…”

Section: Maize Maintenance Methyltransferases Are Highly Expressed Inmentioning

confidence: 99%

“…When cells stop expanding and reach their mature size, they become part of the mature zone (MZ; Nelissen et al, 2013). Previous work has shown that the size of the DZ largely determines final leaf size (Rymen et al, 2007;Nelissen et al, 2012). Here, we use the growth zone of the maize leaf to study the dynamics of DNA methylation during leaf growth by methylation-sensitive amplified polymorphism (MSAP) analysis on dividing, transitioning, elongating, and mature cells.…”

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Differential Methylation during Maize Leaf Growth Targets Developmentally Regulated Genes

et al. 2014

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DNA methylation is an important and widespread epigenetic modification in plant genomes, mediated by DNA methyltransferases (DMTs). DNA methylation is known to play a role in genome protection, regulation of gene expression, and splicing and was previously associated with major developmental reprogramming in plants, such as vernalization and transition to flowering. Here, we show that DNA methylation also controls the growth processes of cell division and cell expansion within a growing organ. The maize (Zea mays) leaf offers a great tool to study growth processes, as the cells progressively move through the spatial gradient encompassing the division zone, transition zone, elongation zone, and mature zone. Opposite to de novo DMTs, the maintenance DMTs were transcriptionally regulated throughout the growth zone of the maize leaf, concomitant with differential CCGG methylation levels in the four zones. Surprisingly, the majority of differentially methylated sequences mapped on or close to gene bodies and not to repeat-rich loci. Moreover, especially the 59 and 39 regions of genes, which show overall low methylation levels, underwent differential methylation in a developmental context. Genes involved in processes such as chromatin remodeling, cell cycle progression, and growth regulation, were differentially methylated. The presence of differential methylation located upstream of the gene anticorrelated with transcript expression, while gene body differential methylation was unrelated to the expression level. These data indicate that DNA methylation is correlated with the decision to exit mitotic cell division and to enter cell expansion, which adds a new epigenetic level to the regulation of growth processes.DNA methylation is the covalent modification of nucleotides in DNA by the addition of a methyl group. In the nuclear genome of higher eukaryotes, 5-methylcytosine is the most important DNA modification (Goll and Bestor, 2005). It is a phenomenon of ancient origin predating plant-animal diversification. However, some differences exist between plant and animal methylome patterning and function, and DNA methylation has been found to be evolutionarily lost in a few species (Feng et al., 2010;Zemach et al., 2010). Eukaryotic DNA methylation is established by DNA methyltransferase (DMT) enzymes that transfer a methyl group from S-adenosyl Met to the fifth carbon of cytosine. These enzymes can largely be subdivided in maintenance and de novo DMTs, depending on whether the recognition site is already methylated or not. Maintenance DMTs conserve the methylation status of symmetrical (palindromic) sites after DNA replication, by recognizing the hemimethylated locus and methylating the newly synthesized strand. In plants, there are two types of maintenance DMTs: DNA METHYLTRANSFERASE (MET) and CHROMOMETHYLASE (CMT). The former methylates CG sites during DNA replication, whereas the latter methylates CHG (H = A, C, or T) sites located in chromatin in which histone 3 is dimethylated on Lys-9 (Goll and Bestor, 2005). De no...

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“…The developmental gradient in growing maize leaves and the large size of the leaf makes it possible to dissect these specific growth zones for further analysis . Since it was recently suggested that it is the final number of cells that primarily determines final leaf size (Gonzalez et al, 2010;Nelissen et al, 2012), we focus our transcriptome analysis specifically on proliferative tissue of the growing leaf.…”

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Combined Large-Scale Phenotyping and Transcriptomics in Maize Reveals a Robust Growth Regulatory Network

et al. 2016

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Leaves are vital organs for biomass and seed production because of their role in the generation of metabolic energy and organic compounds. A better understanding of the molecular networks underlying leaf development is crucial to sustain global requirements for food and renewable energy. Here, we combined transcriptome profiling of proliferative leaf tissue with indepth phenotyping of the fourth leaf at later stages of development in 197 recombinant inbred lines of two different maize (Zea mays) populations. Previously, correlation analysis in a classical biparental mapping population identified 1,740 genes correlated with at least one of 14 traits. Here, we extended these results with data from a multiparent advanced generation intercross population. As expected, the phenotypic variability was found to be larger in the latter population than in the biparental population, although general conclusions on the correlations among the traits are comparable. Data integration from the two diverse populations allowed us to identify a set of 226 genes that are robustly associated with diverse leaf traits. This set of genes is enriched for transcriptional regulators and genes involved in protein synthesis and cell wall metabolism. In order to investigate the molecular network context of the candidate gene set, we integrated our data with publicly available functional genomics data and identified a growth regulatory network of 185 genes. Our results illustrate the power of combining in-depth phenotyping with transcriptomics in mapping populations to dissect the genetic control of complex traits and present a set of candidate genes for use in biomass improvement

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A Local Maximum in Gibberellin Levels Regulates Maize Leaf Growth by Spatial Control of Cell Division

Cited by 74 publications

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Regulatory modules controlling maize inflorescence architecture

Regulatory modules controlling maize inflorescence architecture

Differential Methylation during Maize Leaf Growth Targets Developmentally Regulated Genes

Combined Large-Scale Phenotyping and Transcriptomics in Maize Reveals a Robust Growth Regulatory Network

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