Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships

Albert, Patrice S.; Zhang, Tao; Semrau, Kassandra; Rouillard, Jean-Marie; Kao, Yu-Hsin; Wang, Rachel; Danilova, Tatiana; Jiang, Jiming; Birchler, James A.

doi:10.1073/pnas.1813957116

Cited by 100 publications

(70 citation statements)

References 54 publications

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“…Chromosome painting allows the identification and tracking of the target chromosome at different stages of mitosis and meiosis (Han et al, 2015). Oligo-based chromosome painting probes have been developed in an increasing number of plant species (Han et al, 2015;Qu et al, 2017;Braz et al, 2018;He et al, 2018;Hou et al, 2018;Meng et al, 2018;Albert et al, 2019), and have been used in various cytogenetic and genome studies (Jiang, 2019).…”

Section: Introductionmentioning

confidence: 99%

An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting

Xin

Zhang

et al. 2019

The Plant Journal

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Summary The karyotype represents the basic genetic make‐up of a eukaryotic species. Comparative cytogenetic analysis of related species based on individually identified chromosomes has been conducted in only a few plant groups and not yet in woody plants. We have developed a complete set of 19 chromosome painting probes based on the reference genome of the model woody plant Populus trichocarpa. Using sequential fluorescence in situ hybridization we were able to identify all poplar chromosomes in the same metaphase cells, which led to the development of poplar karyotypes based on individually identified chromosomes. We demonstrate that five Populus species, belonging to five different sections within Populus, have maintained a remarkably conserved karyotype. No inter‐chromosomal structural rearrangements were observed on any of the 19 chromosomes among the five species. Thus, the chromosomal synteny in Populus has been remarkably maintained after nearly 14 million years of divergence. We propose that the karyotypes of woody species are more stable than those of herbaceous plants since it may take a longer period of time for woody plants to fix chromosome number or structural variants in natural populations.

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Section: Introductionmentioning

confidence: 99%

An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting

Xin

Zhang

et al. 2019

The Plant Journal

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“…Although the L-RLK-CML is the strongest candidate for conferring the major effect of QTL10 against C. zeina, it is possible that the QDR may depend on another of the candidates identified in this study. Even though their closest B73 match is not positioned within the QTL region, these candidates may actually be within the QTL in CML444 due to differences in genomic organization compared to B73 (Albert et al, 2019). It is also feasible that the QTL is made up of a combination of tightly linked genes (Nelson et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

De novo Assembly of Transcriptomes From a B73 Maize Line Introgressed With a QTL for Resistance to Gray Leaf Spot Disease Reveals a Candidate Allele of a Lectin Receptor-Like Kinase

et al. 2020

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Gray leaf spot (GLS) disease in maize, caused by the fungus Cercospora zeina, is a threat to maize production globally. Understanding the molecular basis for quantitative resistance to GLS is therefore important for food security. We developed a de novo assembly pipeline to identify candidate maize resistance genes. Near-isogenic maize lines with and without a QTL for GLS resistance on chromosome 10 from inbred CML444 were produced in the inbred B73 background. The B73-QTL line showed a 20% reduction in GLS disease symptoms compared to B73 in the field (p = 0.01). B73-QTL leaf samples from this field experiment conducted under GLS disease pressure were RNA sequenced. The reads that did not map to the B73 or C. zeina genomes were expected to contain novel defense genes and were de novo assembled. A total of 141 protein-coding sequences with B73-like or plant annotations were identified from the B73-QTL plants exposed to C. zeina. To determine whether candidate gene expression was induced by C. zeina, the RNAseq reads from C. zeina-challenged and control leaves were mapped to a master assembly of all of the B73-QTL reads, and differential gene expression analysis was conducted. Combining results from both bioinformatics approaches led to the identification of a likely candidate gene, which was a novel allele of a lectin receptor-like kinase named L-RLK-CML that (i) was induced by C. zeina, (ii) was positioned in the QTL region, and (iii) had functional domains for pathogen perception and defense signal transduction. The 817AA L-RLK-CML protein had 53 amino acid differences from its 818AA counterpart in B73. A second "B73like" allele of L-RLK was expressed at a low level in B73-QTL. Gene copy-specific RT-qPCR confirmed that the l-rlk-cml transcript was the major product induced fourfold by C. zeina. Several other expressed defense-related candidates were identified, including a wall-associated kinase, two glutathione s-transferases, a chitinase, a glucan Frontiers in Plant Science | www.frontiersin.org 1 March 2020 | Volume 11 | Article 191Welgemoed et al.Maize de novo Transcriptome QDR GLS beta-glucosidase, a plasmodesmata callose-binding protein, several other receptorlike kinases, and components of calcium signaling, vesicular trafficking, and ethylene biosynthesis. This work presents a bioinformatics protocol for gene discovery from de novo assembled transcriptomes and identifies candidate quantitative resistance genes.

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“…As in complex centromeres, these edge sequences might have a smaller RT shift than internal sequences. Future cytological experiments, using a combination of flow sorted EdU-labeled nuclei and techniques for identifying maize chromosomes [93,94] could help address questions related to the RT of simple centromeres.…”

Section: Discussionmentioning

confidence: 99%

“…As a result, understanding of such critical areas has lagged behind that in yeast and animal systems. However, with recent progress in assembling genomic resources and anticipated advances in the ability to isolate individual cell types [108], perform sophisticated analyses of genome conformation [109,110] and follow individual chromosome regions using elegant cytological paints [94], the maize root tip system is poised to contribute to rapid progress in these and many other important areas of plant genome biology.…”

Section: Discussionmentioning

confidence: 99%

Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Wear

Song

Zynda

et al. 2020

Preprint

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39 Plant cells undergo two types of cell cycles -the mitotic cycle in which DNA replication is 40 coupled to mitosis, and the endocycle in which DNA replication occurs in the absence of cell 41 division. To investigate DNA replication programs in these two types of cell cycles, we pulse 42 labeled intact root tips of maize (Zea mays) with 5-ethynyl-2'-deoxyuridine (EdU) and used flow 43 sorting of nuclei to examine DNA replication timing (RT) during the transition from a mitotic 44 cycle to an endocycle. Here, we compare sequence-based RT profiles and found that most 45 regions of the maize genome replicate at the same time during S phase in mitotic and 46 endocycling cells, despite the need to replicate twice as much DNA in the endocycle. However, 47 regions collectively corresponding to 2% of the genome displayed significant changes in timing 48 between the two types of cell cycles. The majority of these regions are small, with a median size 49 of 135 kb, and shift to a later RT in the endocycle. However, we found larger regions that shifted 50 RT in centromeres of seven of the ten maize chromosomes. These regions covered the majority 51 of the previously defined functional centromere in each case, which are ~1-2 Mb in size in the 52 reference genome. They replicate mainly during mid S phase in mitotic cells, but primarily in 53 late S phase of the endocycle. Strikingly, the immediately adjacent pericentromere sequences are 54 primarily late replicating in both cell cycles. Analysis of CENH3 enrichment levels in nuclei of 55 different ploidies suggested that there is only a partial replacement of CENH3 nucleosomes after 56 endocycle replication is complete. The shift to later replication of centromeres and reduced 57 CENH3 enrichment after endocycle replication is consistent with the hypothesis that centromeres 58 are being inactivated as their function is no longer needed. Wear et al. 3 59 AUTHOR SUMMARY60 In traditional cell division, or mitosis, a cell's genetic material is duplicated and then split 61 between two daughter cells. In contrast, in some specialized cell types, the DNA is duplicated a 62 second time without an intervening division step, resulting in cells that carry twice as much DNA 63 -a phenomenon called an endocycle, which is common during plant development. At each step, 64 DNA replication follows an ordered program, in which highly compacted DNA is unraveled and 65 replicated in sections at different times during the synthesis (S) phase. In plants, it is unclear 66 whether traditional and endocycle programs are the same. Using root tips of maize, we found a 67 small portion of the genome whose replication in the endocycle is shifted in time, usually to later 68 in S phase. Some of these regions are scattered around the genome, and mostly coincide with 69 active genes. However, the most prominent shifts occur in centromeres. This location is 70 noteworthy because centromeres orchestrate the process of separating duplicated chromosomes 71 into daughter cells, a function that is not needed in...

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Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships

Cited by 100 publications

References 54 publications

An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting

An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting

De novo Assembly of Transcriptomes From a B73 Maize Line Introgressed With a QTL for Resistance to Gray Leaf Spot Disease Reveals a Candidate Allele of a Lectin Receptor-Like Kinase

Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

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