Domestication, polyploidy and genomics of crops and weeds PAGXXV

Plant and Animal Genome Conference in San Diego #PAGXXV each January is the chance to join 3500 people working in genomics. I presented a talk on the molecular cytogenetics group’s work, starting with consideration of early stages of crop domestication, and then thinking about how we can make agriculture more sustainable. I also considered weeds, noting that they have been co-domesticated with crops by people, being under strong selection pressure and exploiting ecological niches coming from the activity of people.

Here are the slides for my talk which are on slideshare at http://www.slideshare.net/PatHeslopHarrison/domestication-polyploidy-and-genomics-of-crops-pagxxv-heslopharrison

Domestication, polyploidy and genomics of crops #PAGXXV Heslop-Harrison from Pat (JS) Heslop-Harrison

Domestication, polyploidy and genomics of crops #PAGXXV Heslop-Harrison from Pat (JS) Heslop-Harrison

This is the text on the slides:

  1. 1. Domestication, polyploidy and genomics of crops (and weeds) Pat Heslop-Harrison & Trude Schwarzacher Leicester, UK phh@molcyt.com http://www.molcyt.com http://www.molcyt.org Twitter Pathh1 . Crop Evolution Genomics & Future Agricultural Productivity PAGXXV 14 January 2017 20 min talk
  2. 2. Outputs –Crops (Chemical energy) – Food – Feed – Fuel – Fibre – Flowers – Pharmaceuticals – Fun2
  3. 3. Inputs –Light –Heat –Water –Gasses –Nutrients –Light –Heat –Water –Gasses –Nutrients (Ecosystem services) Outputs –CROPS – Chemical energy
  4. 4. Domestication, Polyploidy and Genomics of Crops • CROPS: where one species controls the growth and reproduction of another
  5. 5. Domestication, Polyploidy and Genomics of Crops • Most species domesticated 10,000 years ago (cereals, legumes/pulses, brassicas, fruits, cows/sheep/pigs, silkworm/bees) • Few species more recently (rabbits, fish, trees, biofuel crops) • A few dropped out of production • First steps: productive, reproduce easily, disease- free, edible/tasty, harvestable … • With critical technology of people: not obvious Heslop-Harrison & Schwarzacher Domestication genomics in Arie Altman http://www.tinyurl.com/domest and review of rabbits http://www.tinyurl.com/rabdom
  6. 6. Pinus sylvestris Scots pine
  7. 7. Argemone mexicana
  8. 8. Japanese knotweed – invasive in Europe Fallopia (and Fallopia x Muehlenbeckia hybrids)
  9. 9. Larrea tridenta Creosote bush
  10. 10. Domestication, polyploidy and genomics of crops and weeds • CROPS: where one species controls the growth and reproduction of another • WEEDS • Many animals collect food to see them through the winter, build nests in anticipation of reproduction • A few plants kill off all others nearby • Ants (Formicidae) farm plants, animals and fungi • Humans only for 20% of their history – and still exploiting environment unsustainably!
  11. 11. Organelle sequences from chloroplasts or mitochondria Sequences from viruses Transgenes introduced with molecular biology methods Genes, regulatory and non- coding low-copy sequences Dispersed repeats Repetitive DNA sequences Nuclear Genome Tandem repeats Satellite sequences DNA transposonsRetrotransposons Centromeric repeats Structural components of chromosomes Telomeric repeats Simple sequence repeats or microsatellites Repeated genes Subtelomeric repeats 45S and 5S rRNA genes Blocks of tandem repeats at discrete chromosomal loci DNA sequence components of the nuclear genome After Biscotti et al. Chromosome Research 2015 Other genes Transposable elements Autonomous/ non-autonomous Dispersed repeats that we don’t know about – except each is significant proportion of genome
  12. 12. Genomic Components: properties • Tandem Repeats • Simple Sequence Repeats • Dispersed Repeats • Functional Repeats • Retroelements • Genes Typical Fraction 10% 5% 10% 15% 50% 10%
  13. 13. Domestication, polyploidy and genomics of crops and weeds • Genome size • Critical parameter for genome studies – first sequenced genomes chosen to be small … Large genomes only tackled 25 years on • But is it critical for species … • No: you can’t ‘look’ at a species and make any suggestion about it’s genome size …
  14. 14. Nothing special about crop genomes? Crop Genome size 2n Ploidy Food Rice 400 Mb 24 2 Triploid endosperm Wheat 17,000 Mbp 42 6 Triploid endosperm Maize 950 Mbp 10 4 (palaeo-tetraploid) Triploid endosperm Rapeseed B. napus 1125 Mbp 38 4 Cotyledon oil/protein Sugar beet 758 Mbp 18 2 Modified root Cassava 770 Mbp 36 2 Tuber Soybean 1,100 Mbp 40 4 Seed cotyledon Oil palm 3,400 Mbp 32 2 Fruit mesocarp Banana 500 Mbp 33 3 Fruit mesocarp Heslop-Harrison & Schwarzacher 2012. Tinyurl.com/domest
  15. 15. Domestication, polyploidy and genomics of crops and weeds • Polyploidy is also critical part of genomes … • No: you can’t ‘look’ at a species and make any suggestion about it’s ploidy …
  16. 16. D’Hont et al. Nature 2012 doi:10.1038/nature11241
  17. 17. D’Hont et al. Nature 2012 doi:10.1038/na ture11241 Whole-genome duplication events.
  18. 18. Domestication, polyploidy and genomics of crops and weeds • Ancient polyploidy (detected by sequencing) • Modern polyploidy (detected by cytogenetics) • Advantages: more control, genes free to mutate, ?larger cells/organs • Disadvantages: meiosis challenging, buffering of changes, more DNA to replicate
  19. 19. Repetitive DNA in dandelion 3 microspecies 22, 12 & 12 Gb 2n=3x=24 apomictic Rubar Salih & Lubos Majesky
  20. 20. k-mer analysis For a 16-mer length, there are 2 billion canonical 16-mers (416/2), and the average 16-mer occurs 10 times in the 22Gb of sequence data. The overall distribution of these informs us about how repetitive the genome is, and the frequency of different repetitive elements.
  21. 21. k-mer analysis The most abundant 16-mers in the 150bp genome reads: 7bp telomere sequence (TTTAGGG/CCCTAAA) added ends of each chromosome occurs a total of 7M times, much higher than the expectation of 140. From 128-mer GT10kb Coverage Depth = 7 AF(11)_S983_009 Blue: DAPI fluorescence. Green: telomere primer HC_89bp Red: 5S rDNA
  22. 22. In asexual dandelion microspecies Rubar M. Salih Genome evolution and biodiversity •Actively evolving repetitive sequences in the genome •Differences seen between microspecies in repeats •Structural and mobile components of genome identified •Chloroplast sequence gives phylogeny and robust markers for diversity (PLoS One in press Dec 2016)
  23. 23. So questions are 1) where is this sequence located in the genome? and 2) are there any differences between the microspecies in its abundance? We can see this is a Ty1-Copia element because the retroelements coding domains are in the order RNaseH Reverse Transcriptase Integrase LTRs divergent More (solo LTRs) RepeatExplorer: Graph-based clustering of related sequences, program/approach by Novák P, Neumann P, Pech J, Steinhaisl J, Macas J. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013 Mar 15;29(6):792-3.
  24. 24. Widely dispersed distribution of a copia retroelement family over all chromosomes of Taraxacum Retrotransposons in Taraxacum 2n=3x=24 NOR sats shown
  25. 25. Distribution from RepeatExplorer O978 the top 10 in terms of genome% and nature of sequence – for each of the three spp. # TxS3 TxA978 TxO978 Repeat masker Genome % Repeat masker Genome % Repeat masker Genome % 1 Low complexity 1.60 Low complexity 0.965 Simple repeat 1.400 2 Low complexity 1.26 Low complexity 0.818 LTR.Gypsy 1.250 3 LTR.Gypsy 1.22 LTR.Gypsy 0.807 Simple repeat 1.200 4 LTR.Gypsy 1.17 Low complexity 0.796 Low complexity 0.963 5 Low_complexity 1.09 Low complexity 0.788 LTR.Gypsy 0.845 6 LTR.Copia 1.04 Low complexity 0.771 Low complexity 0.820 7 LTR.Gypsy 0.995 LTR.Gypsy 0.730 LTR.Gypsy 0.793 8 Low_complexity 0.982 Low complexity 0.713 Low complexity 0.781 9 LTR.Gypsy 0.940 LTR.Gypsy 0.682 LTR.Gypsy 0.741 10 LTR.Copia 0.841 Low complexity 0.671 Low complexity 0.724 S3 A978 Petunia
  26. 26. Relative counts of various k- mers in three Taraxacum microspecies Rubar Salih et al. in prep
  27. 27. Dispersed on chromosomes in all microspecies: but differences AA1_AK07_171D_45S B_010 AC1_O996_171 D_KsHC B_003AC11_S933_171 D_KsHC B_004 0.075% Low complexity Assembled to genome of: A: S: O:
  28. 28. Sequence CL80 double-dots on 14 chromosomes (not 16 – not 2 genomes worth) – is it a centromeric repeat? LTR.Copia (2hits, 0.103%) Low complexity (5hits, 0.0895%) Genome proportion = 0.2480% Assembled to genome: A = S = O = AE (3)_A978_A dig_pta794_001 AE (4)_O976_A dig_pta794_002 AE (2)_S3_A dig_Pta794 bio_002
  29. 29. Unknown or Chloroplast Low Complexity Mixed Repeat LTR Degenerate LTR Gypsy LTR Copia DNA Transposons LINES LTR Caulimovirus Simple Repeat rRNA Tandem Repeat Telomere Genomeproportion(%) Cluster (number) I I I I I I I I 1 50 100 150 200 250 300 351 Telomere Tandem Repeat rRNA Simple Repeat LTR Caulimovirus LINES DNA Transposons LTR Copia LTR Gypsy LTR Degenerate Mixed Repeat Low Complexity Unknown or Chloroplast Retroelements and tandem repeats in Petunia Supplementary Ms 2. Bombarely et al. Petunia genome sequence Nature Plants 2: article number 16074. Telomere Tandem Repeat rRNA Simple Repeat LTR Caulimovirus LINES DNA Transposons LTR Copia LTR Gypsy LTR Degenerate Mixed Repeat Low Complexity Unknown or Chloroplast
  30. 30. Organelle sequences from chloroplasts or mitochondria Sequences from viruses Transgenes introduced with molecular biology methods Genes, regulatory and non- coding low-copy sequences Dispersed repeats Repetitive DNA sequences Nuclear Genome Tandem repeats Satellite sequences DNA transposonsRetrotransposons Centromeric repeats Structural components of chromosomes Telomeric repeats Simple sequence repeats or microsatellites Repeated genes Subtelomeric repeats 45S and 5S rRNA genes Blocks of tandem repeats at discrete chromosomal loci DNA sequence components of the nuclear genome After Biscotti et al. Chromosome Research 2015 Other genes Transposable elements Autonomous/ non-autonomous Dispersed repeats that we don’t know about – except each is significant proportion of genome
  31. 31. Japanese knotweed – invasive in watercourses in Europe Fallopia (and Fallopia x Muehlenbeckia hybrids)
  32. 32. Repeat Explorer analysis raw reads of F. japonica and M. australis. Top clusters represented 50% of the reads in F. japonica and 39.5% of reads in M. australis. F. japonica has a higher proportion of dispersed repeats than M. australis.
  33. 33. Fallopia x Muehlenbeckia hybrid : Differential probes identified by k-mer and RepeatExplorer Green is Fallopia-specific; Red is equal in both genomes Desjardins, Bailey, Wang, Schwarzacher, Heslop-Harrison. 2017 in prep
  34. 34. Desjardins, Bailey, Wang, Schwarzacher, Heslop-Harrison. 2017 in prep.
  35. 35. Panicum sensu stricto c. 100 species; x=9 Evolution of Panicum miliaceum Proso millet P. miliaceum 2n=4x=36 P. capillare 2n=2x=18 P. repens 2n=4x=36 also 2n=18 to 54 P. sumatrense 2n=2x=18 or 4x=36 Global North-temperate Low genetic diverstiy Weedy forms P. virgatum 2n=4x=36 or 2x=18 ? ? ? ? ?? • Hunt , HH et al. 2014. Reticulate evolution in Panicum (Poaceae): the origin of tetraploid broomcorn millet, P. miliaceum. J Exp Bot. 2014
  36. 36. Chromosome and genome engineering Cell fusion hybrid of two 4x tetraploid tobacco species Patel, Badakshi, HH, Davey et al 2011 Annals of Botany
  37. 37. Nicotiana hybrid 4x + 4x cell fusions Each of 4 chromosome sets has distinctive repetitive DNA when probed with genomic DNA Patel et al Ann Bot 2011 Cell fusion hybrid of two 4x tetraploid tobacco species Four genomes differentially labelled Patel, Badakshi, HH, Davey et al 2011 Annals Botany
  38. 38. Wheat evolution and hybrids Triticum uratu 2n=2x=14 AA Einkorn Triticum monococcum 2n=2x=14 AA Bread wheat Triticum aestivum 2n=6x=42 AABBDD Durum/Spaghetti Triticum turgidum ssp durum 2n=4x=28 AABB Triticum dicoccoides 2n=4x=28 AABB Aegilops speltoides relative 2n=2x=14 BB Triticum tauschii (Aegilops squarrosa) 2n=2x=14 DD Triticale xTriticosecale 2n=6x=42 AABBRR Rye Secale cereale 2n=2x=14 RR
  39. 39. Centromere dynamics and timing of chromosome synapsis (6x wheat) Adel Sepsi, Higgins, Heslop‐Harrison, Schwarzacher. CENH3 morphogenesis reveals dynamic centromere associations during synaptonemal complex formation and the progression through male meiosis in hexaploid wheat. Plant Journal. 2016 Sep 1. Sepsi et al. Plant Journal 2016
  40. 40. (b) Centromere depolarisation and SC formation during Zygotene Interphase Leptotene Zygotene Late ZygoteneTelomere bouquet Homologue chromosome pairs Centromeres ZYP1 Early Zygotene 1 2 3 Subtelomeric synapsis Interstitial alignment Interstitial elongation (a) Centromere, telomere and chromosome arm dynamics in meiotic prophase I. Sepsi et al. Plant Journal 2016
  41. 41. How do genomes evolve? –Gene mutation very rarely • (human: 10−8 /site/generation) –Chromosome evolution –Polyploidy and genome duplication –Repetitive sequences: mobility & copy number • (10−4 /generation in µsat) –Recombination –Epigenetic aspects: centromeres & expression
  42. 42. Repetitive sequences • Many families and various types • Abundant • Rapidly evolving … or conserved – Copy number and sequence • May be near-genome specific, even chromosome-specific • Various genome/chromosomal locations
  43. 43. Organelle sequences from chloroplasts or mitochondria Sequences from viruses Transgenes introduced with molecular biology methods Genes, regulatory and non- coding low-copy sequences Dispersed repeats Repetitive DNA sequences Nuclear Genome Tandem repeats Satellite sequences DNA transposonsRetrotransposons Centromeric repeats Structural components of chromosomes Telomeric repeats Simple sequence repeats or microsatellites Repeated genes Subtelomeric repeats 45S and 5S rRNA genes Blocks of tandem repeats at discrete chromosomal loci DNA sequence components of the nuclear genome After Biscotti et al. Chromosome Research 2015 Other genes Transposable elements Autonomous/ non-autonomous Dispersed repeats that we don’t know about – except each is significant proportion of genome
  44. 44. Sequences from viruses Transgenes introduced with molecular biology methods Genes, regulatory and non- coding low-copy sequences Dispersed repeats Repetitive DNA sequences Nuclear Genome Tandem repeats Satellite sequences DNA transposonsRetrotransposons Centromeric repeats Structural components of chromosomes Telomeric repeats Simple sequence repeats or microsatellites Repeated genes Subtelomeric repeats 45S and 5S rRNA genes Blocks of tandem repeats at discrete chromosomal loci Real? Passively Amplified DNA sequences: PADs Or: Transposable element derivatives (LTRs etc)? Other genes Transposable elements Autonomous/ non-autonomous Dispersed repeats that we don’t know about – except each is significant proportion of genome
  45. 45. Domestication, polyploidy and genomics of crops (and weeds) Pat Heslop-Harrison & Trude Schwarzacher and collaborators Leicester, UK phh@molcyt.com http://www.molcyt.com http://www.molcyt.org Twitter Pathh1 .
  46. 46. From Chromosome to Nucleus Pat Heslop-Harrison phh4@le.ac.uk http://www.molcyt.com
  47. 47. • About half of all higher plant species are recognizable as polyploids, a major feature of genome architecture where there are more than two sets of chromosomes. Advantages include multiple copies of each gene with different regulation, so essentially fixing heterosis; larger cell size; and the opportunity for mutation without lethality. Disadvantages include twice as much DNA to replicate; incorrect control of multiple gene copies in interacting genomes; chromosome instability at mitosis; and the challenges of ensuring chromosome pairing and regular meiotic segregation in seed crops, in breeding hybrid materials, or else combining sterility with parthenocarpy in fruit crops. Given these substantial contrasts, it is perhaps surprising that the top three cereal crops are wheat (a modern hexaploid 2n=6x=42), rice (diploid, 2n=2x=14), and maize (palaeotetraploid, 2n= 2 or 4 x =20), suggesting neither advantages nor disadvantages are overwhelming. I will consider the balance of positives and negatives over evolutionary and crop-breeding timescales. In the second part of my talk, I will consider how knowledge of polyploid behaviour and knowledge of ancestors can be exploited, discussing our work with polyploids, both well-known (wheat, Brassica, banana) and less known (proso millet, ornamentals and saffron crocus). Further details and references will be at http://www.molcyt.com. Email phh(a)molcyt.com

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About Pat Heslop-Harrison

Professor of Molecular Cytogenetics and Cell Biology, University of Leicester Chief Editor, Annals of Botany. Research: genome evolution, breeding and biodiversity in agricultural species; the impact of agriculture; evalutation of research and advanced training.
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