Stomata, which are epidermal pores surrounded by two guard cells, develop from a specialized stem cell lineage and function in shoot gas exchange. The Arabidopsis thaliana FOUR LIPS (FLP) and MYB88 genes encode closely related and atypical two-MYB-repeat proteins, which when mutated result in excess divisions and abnormal groups of stomata in contact. Consistent with a role in transcription, we show here that FLP and MYB88 are nuclear proteins with DNA binding preferences distinct from other known MYBs. To identify possible FLP/MYB88 transcriptional targets, we used chromatin immunoprecitation (ChIP) followed by hybridization to Arabidopsis whole genome tiling arrays. These ChIP-chip data indicate that FLP/MYB88 target the upstream regions especially of cell cycle genes, including cyclins, cyclin-dependent kinases (CDKs), and components of the prereplication complex. In particular, we show that FLP represses the expression of the mitosis-inducing factor CDKB1;1, which, along with CDKB1;2, is specifically required both for the last division in the stomatal pathway and for cell overproliferation in flp mutants. We propose that FLP and MYB88 together integrate patterning with the control of cell cycle progression and terminal differentiation through multiple and direct cell cycle targets. FLP recognizes a distinct cis-regulatory element that overlaps with that of the cell cycle activator E2F-DP in the CDKB1;1 promoter, suggesting that these MYBs may also modulate E2F-DP pathways.
In multicellular organisms, morphogenesis relies on a strict coordination in time and space of cell proliferation and differentiation. In contrast to animals, plant development displays continuous organ formation and adaptive growth responses during their lifespan relying on a tight coordination of cell proliferation. How developmental signals interact with the plant cell-cycle machinery is largely unknown. Here, we characterize plant A2-type cyclins, a small gene family of mitotic cyclins, and show how they contribute to the fine-tuning of local proliferation during plant development. Moreover, the timely repression of CYCA2;3 expression in newly formed guard cells is shown to require the stomatal transcription factors FOUR LIPS/MYB124 and MYB88, providing a direct link between developmental programming and cell-cycle exit in plants. Thus, transcriptional downregulation of CYCA2s represents a critical mechanism to coordinate proliferation during plant development.
BackgroundStability of multiple testing procedures, defined as the standard deviation of total number of discoveries, can be used as an indicator of variability of multiple testing procedures. Improving stability of multiple testing procedures can help to increase the consistency of findings from replicated experiments. Benjamini-Hochberg’s and Storey’s q-value procedures are two commonly used multiple testing procedures for controlling false discoveries in genomic studies. Storey’s q-value procedure has higher power and lower stability than Benjamini-Hochberg’s procedure. To improve upon the stability of Storey’s q-value procedure and maintain its high power in genomic data analysis, we propose a new multiple testing procedure, named Bon-EV, to control false discovery rate (FDR) based on Bonferroni’s approach.ResultsSimulation studies show that our proposed Bon-EV procedure can maintain the high power of the Storey’s q-value procedure and also result in better FDR control and higher stability than Storey’s q-value procedure for samples of large size(30 in each group) and medium size (15 in each group) for either independent, somewhat correlated, or highly correlated test statistics. When sample size is small (5 in each group), our proposed Bon-EV procedure has performance between the Benjamini-Hochberg procedure and the Storey’s q-value procedure. Examples using RNA-Seq data show that the Bon-EV procedure has higher stability than the Storey’s q-value procedure while maintaining equivalent power, and higher power than the Benjamini-Hochberg’s procedure.ConclusionsFor medium or large sample sizes, the Bon-EV procedure has improved FDR control and stability compared with the Storey’s q-value procedure and improved power compared with the Benjamini-Hochberg procedure. The Bon-EV multiple testing procedure is available as the BonEV package in R for download at https://CRAN.R-project.org/package=BonEV.Electronic supplementary materialThe online version of this article (doi:10.1186/s12859-016-1414-x) contains supplementary material, which is available to authorized users.
Functional centromeres, the chromosomal sites of spindle attachment during cell division, are marked epigenetically by the centromerespecific histone H3 variant cenH3 and typically contain long stretches of centromere-specific tandem DNA repeats (∼1.8 Mb in maize). In 23 inbreds of domesticated maize chosen to represent the genetic diversity of maize germplasm, partial or nearly complete loss of the tandem DNA repeat CentC precedes 57 independent cenH3 relocation events that result in neocentromere formation. Chromosomal regions with newly acquired cenH3 are colonized by the centromere-specific retrotransposon CR2 at a rate that would result in centromere-sized CR2 clusters in 20,000-95,000 y. Three lines of evidence indicate that CentC loss is linked to inbreeding, including (i) CEN10 of temperate lineages, presumed to have experienced a genetic bottleneck, contain less CentC than their tropical relatives; (ii) strong selection for centromere-linked genes in domesticated maize reduced diversity at seven of the ten maize centromeres to only one or two postdomestication haplotypes; and (iii) the centromere with the largest number of haplotypes in domesticated maize (CEN7) has the highest CentC levels in nearly all domesticated lines. Rare recombinations introduced one (CEN2) or more (CEN5) alternate CEN haplotypes while retaining a single haplotype at domestication loci linked to these centromeres. Taken together, this evidence strongly suggests that inbreeding, favored by postdomestication selection for centromere-linked genes affecting key domestication or agricultural traits, drives replacement of the tandem centromere repeats in maize and other crop plants. Similar forces may act during speciation in natural systems.centromere drive | centromere paradox | founder effect | hemicentric inversion | linkage disequilibrium C entromere-specific tandemly arranged DNA repeats vary in length and nucleotide sequence between species. The puzzling observation that centromeres can consist of highly variable sequences despite being involved in an essential cellular function (i.e., chromosome segregation) has been coined the "centromere paradox" (1). "Centromere drive" has been proposed to preferentially segregate the "favored" centromere into the female gamete and thereby provide the selective force that acts on centromere DNA sequences and interacting proteins (2).Maize (Zea mays ssp. mays) was domesticated between 7.5 and 10 thousand years ago (ka) from wind-pollinated outcrossing wild teosinte (Z. mays ssp. parviglumis) (3, 4) in a process that dramatically changed its morphology. Several quantitative trait loci (QTLs) responsible for these morphological changes were identified in pioneering work (5-8), and a large number of additional genetic loci involved in maize domestication and improvement were subsequently identified in genome-wide scans (9). Gene (and centromere) flow between the fully interfertile maize and teosinte subspecies has been documented (10, 11). Functional centromeres of maize consist of 1-2 Mb of DN...
SUMMARYStomata are vital for the adaptation of plants to abiotic stress, and in turn stomatal density is modulated by environmental factors. Less clear, however, is whether regulators of stomatal development themselves participate in the sensing or response of stomata to abiotic stress. FOUR LIPS (FLP) and its paralog MYB88 encode MYB proteins that establish stomatal patterning by permitting only a single symmetric division before stomata differentiate. Hence, flp-1 myb88 double mutants have an excess of stomata, which are often misplaced in direct contact. Here, we investigate the consequences of loss of FLP/MYB88 function on the ability of Arabidopsis plants to respond to abiotic stress. While flp-1 myb88 double mutants are viable and display no obvious aerial phenotypes under normal greenhouse growth conditions, we show that flp-1 myb88 plants are significantly more susceptible to drought and high salt, and have increased rates of water loss. To determine whether flp-1 myb88 plants are already challenged under normal growth conditions, we compared genome-wide transcript levels between flp-1 myb88 and wild-type green tissues. Unexpectedly, uninduced flp-1 myb88 plants showed a reduced accumulation of many typical abiotic stress gene transcripts. Moreover, the induction of many of these stress genes under high-salt conditions was significantly lower in flp-1 myb88 plants. Our results provide evidence for a new function of FLP/MYB88 in sensing and/or transducing abiotic stress, which is severely compromised in flp-1 myb88 mutants.
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