1. Chromosomes and Gene Expression
  2. Genetics and Genomics

Meiotic drive of female-inherited supernumerary chromosomes in a pathogenic fungus

  1. Michael Habig
  2. Gert HJ Kema
  3. Eva Holtgrewe Stukenbrock  Is a corresponding author
  1. Christian-Albrechts University of Kiel, Germany
  2. Max Planck Institute for Evolutionary Biology, Germany
  3. Wageningen University and Research, The Netherlands
https://doi.org/10.7554/eLife.40251
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Cite this article
  1. Michael Habig
  2. Gert HJ Kema
  3. Eva Holtgrewe Stukenbrock
(2018)
Meiotic drive of female-inherited supernumerary chromosomes in a pathogenic fungus
eLife 7:e40251.
https://doi.org/10.7554/eLife.40251
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6 figures, 2 tables and 7 additional files

Figures

Figure 1 with 1 supplement
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Meiosis and chromosome segregation in Z.tritici.

(A) Schematic overview of the assumed sexual process between two parental strains of Z. tritici (Alexopoulos et al., 1996; Kema et al., 2018) with one supernumerary chromosome shared and therefore …

https://doi.org/10.7554/eLife.40251.002
Figure 1—figure supplement 1
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Synteny comparison of IPO94269 and IPO323.

(A) Synteny blot for IPO94269 unitigs on IPO323 chromosomes. (B) Summary table of syntenic regions of IPO323 and IPO94269.

https://doi.org/10.7554/eLife.40251.003
Figure 2 with 1 supplement
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Unpaired supernumerary chromosomes show a segregation advantage only when inherited from the female parent.

(A) Relative frequencies of mitochondrial genotypes in random and randomized ascospores in experiments A, B and C. The mitochondrial transmission varied significantly between the three experiments. …

https://doi.org/10.7554/eLife.40251.004
Figure 2—figure supplement 1
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Transmission of unpaired chromosomes and mitochondria.

(A) Detailed presence/absence frequencies for all unpaired supernumerary chromosomes according to the mitochondrial genotype present in all ascospores. Data for the three experiments A, B and C are …

https://doi.org/10.7554/eLife.40251.005
Figure 3 with 2 supplements
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Paired supernumerary chromosomes show Mendelian segregation with frequent losses.

Analysis of segregation of paired supernumerary chromosomes in 24 complete tetrads. The transmission of chromosomes 14, 15, 16, 17, 19, and 21 with homologs in both parental strains IPO94269 and …

https://doi.org/10.7554/eLife.40251.006
Figure 3—source data 1

Examples of gel electrophoresis of PCR products for (A) core chromosome 13 marker on mating type, (B) core chromosome 4 marker 11O21, (C) core chromosome 4 marker 04L20, (D) core chromosome three marker caa-0002, core chromosome five marker ggc-001, core chromosome seven marker ac-001, (E) segregating marker of the mitochondrial genotype, (F) segregating marker of the supernumerary chromosome 14, (G) segregating marker of the supernumerary chromosome 15, (H) segregating marker of the supernumerary chromosome 16, (I) segregating marker of the supernumerary chromosome 17, (J) segregating marker of the supernumerary chromosome 19, (K) segregating marker of the supernumerary chromosome 19, (L) subtelomeric marker of the supernumerary chromosome 19, (M) subtelomeric marker of the supernumerary chromosome 19, (N) segregating marker of the supernumerary chromosome 21, (O) subtelomeric marker of the supernumerary chromosome 18, (P) centromeric marker of the supernumerary chromosome 18, (Q) subtelomeric marker of the supernumerary chromosome 18, (R) subtelomeric marker of the supernumerary chromosome 20, (S) centromeric marker of the supernumerary chromosome 20, (T) subtelomeric marker of the supernumerary chromosome 20.

https://doi.org/10.7554/eLife.40251.009
Figure 3—figure supplement 1
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Whole genome sequencing confirms chromosome drive for unpaired supernumerary chromosomes.

Coverage heatmap for eight ascospores (T0325-T0332) of ascus A03-4 (A–C) and eight ascospores (T0801-T0808) of ascus A08-1 (D–F). (a) Supernumerary chromosome complement in cross resulting in ascus …

https://doi.org/10.7554/eLife.40251.007
Figure 3—figure supplement 2
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Distribution of SNPs on core and supernumerary chromosomes in two fully sequenced tetrad.

The distribution is consistent with the origin of each tetrad in one meiotic event and Mendelian segregation for core and paired supernumerary chromosomes. (A) Distribution of IPO94269 specific SNP …

https://doi.org/10.7554/eLife.40251.008
Figure 4
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Unpaired supernumerary chromosome show meiotic drive if inherited from the female parent.

Analysis of segregation of unpaired supernumerary chromosomes in 24 complete tetrads according to the mitochondrial genotype. The transmission of chromosomes unique to one of the parental strains …

https://doi.org/10.7554/eLife.40251.010
Figure 5
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Meiotic chromosome drive in Z.tritici.

Schematic illustration depicting two possible mechanisms for the observed meiotic chromosome drive of female derived unpaired supernumerary chromosomes. Light blue/orange: paired supernumerary …

https://doi.org/10.7554/eLife.40251.011
Author response image 1
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IPO94269 specific SNPs with less than four occurrences among the eight ascospores are interspersed among IPO94269 specific SNPs with exactly four occurrences among the eight ascospores.

A) Whole genome view of all eight ascopsores of ascus A03-4. Stretches of IPO94269 haplotype alternate with stretches of IPO323 haplotype. Crossover events are discernible between all eight …

https://doi.org/10.7554/eLife.40251.022

Tables

Table 1
Summary of crosses and progeny generated in this study.
https://doi.org/10.7554/eLife.40251.012
Ascospores
(random*/all)		Verified tetrads
(mtIPO323/mtIPO94269)
#Parental strain 1Parental strain 2Unpaired chr from IPO94269Unpaired chr from IPO323ConditionExp AExp BExp CExp AExp BExp C
 1IPO323IPO94269-chr18, chr20Co-inoculation
107 cells/mL		96/9612/9651/88-2/20
 2IPO323
∆chr14		IPO94269chr14chr18, chr20Co-inoculation
107 cells/mL		96/968/6438/72-3/01/0
 3IPO323
∆chr21		IPO94269chr21chr18, chr20Co-inoculation
107 cells/mL		89/894/3252/78-00
 4IPO323
∆chr16		IPO94269chr16chr18, chr20Co-inoculation
107 cells/mL		96/966/4838/115-1/00/1
 5IPO323
∆chr17		IPO94269chr17chr18, chr20Co-inoculation
107 cells/mL		96/962/1615/59-02/0
 5IPO323
∆chr19		IPO94269chr19chr18, chr20Co-inoculation
107 cells/mL		96/969/7238/77-3/10/1
 7IPO323
∆chr20		IPO94269-chr18Co-inoculation
107 cells/mL		96/964/3219/31-2/00
 8IPO323
∆chr18		IPO94269-chr20Co-inoculation
107 cells/mL		96/964/3230/67-1/02/0
 9IPO323
∆chr15		IPO94269chr15chr18, chr20Co-inoculation
107 cells/mL		96/966/4814/54-1/00/1
 10IPO323
∆chr19		IPO94269chr19chr18, chr20IPO323
106 cells/mL		--25/42--0
 11IPO323
∆chr19		IPO94269chr19chr18, chr20IPO323
105 cells/mL		--38/43--0
 12IPO323
∆chr19		IPO94269chr19chr18, chr20IPO323
104 cells/mL		--2/16--0
 13IPO323
∆chr19		IPO94269chr19chr18, chr20IPO94269
+6dpi		--40/46--0
 14IPO323
∆chr19		IPO94269chr19chr18, chr20IPO94269
+12dpi		--11/11--0
 15IPO323
∆chr19		IPO94269chr19chr18, chr20IPO94269
106 cells/mL		--60/84--0
 16IPO323
∆chr19		IPO94269chr19chr18, chr20IPO94269
105 cells/mL		--48/80--0
 17IPO323
∆chr19		IPO94269chr19chr18, chr20IPO94269
104 cells/mL		--28/28--0
 18IPO323
∆chr19		IPO94269chr19chr18, chr20IPO323
+6pdi		--5/29--0
 19IPO323
∆chr19		IPO94269chr19chr18, chr20IPO323
+12dpi		--51/71--1/0
∑761/76155/440603/1091-13/35/3

  1. *Includes random and randomized ascospores. Randomized ascospores were generated by randomly selecting one ascospore per tetrad.

Table 2
Overview of six segregating markers located on the essential chromosomes.
https://doi.org/10.7554/eLife.40251.013
MarkerLocalization (IPO323)Localization
(IPO94269)		Primer1Primer 2Product size in IPO323 [bp]Product size in IPO94269 [bp]
mat1-1/mat1-2chr13 621930–622924Unitig11
627136–627792		MAT1-1F, MAT1-1RMAT1-2F, MAT1-2R340660
11O21chr4 642791–642996Unitig03
757794–757990		11O21F11O21R205199
04L20chr4
2276298–2276497		Unitig03
2427163–2427370		04L20F04L20R192199
caa-0002chr3
2927294–2927704		Unitig02
566646–567041		29962997412396
ggc-001chr5
1190388–1190640		Unitig04
1143568–1143802		29982999254234
ac-0001chr7
266661–266847		Unitiq05
372979–373151		30003001187173

Additional files

Supplementary file 1

All primers used in this study.

https://doi.org/10.7554/eLife.40251.014
Supplementary file 2

Summary of all PCR marker results for experiment A.

https://doi.org/10.7554/eLife.40251.015
Supplementary file 3

Summary of all PCR marker results for experiment B.

https://doi.org/10.7554/eLife.40251.016
Supplementary file 4

Summary of all PCR marker results for experiment C.

https://doi.org/10.7554/eLife.40251.017
Supplementary file 5

Summary of statistical tests performed in this study.

https://doi.org/10.7554/eLife.40251.018
Supplementary file 6

Frequency of transmission of paired chromosomes to progeny ascospores.

https://doi.org/10.7554/eLife.40251.019
Transparent reporting form
https://doi.org/10.7554/eLife.40251.020

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