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The Environment Institute
                          Where ideas grow




 Richard Abbott

 Plant Introductions & Evolution: Hybrid Speciation and Gene Transfer
Plant Introductions & Evolution:
    Hybrid Speciation and
          Gene Transfer




   Richard Abbott - St Andrews University, UK
“There are almost 11,000 alien species in
 Europe and the trend of new arrivals is
 showing no signs of levelling out.”


   “…approximately 15% of the aliens within Europe
     are known to have some impact on the
     environment or economy - and this problem
     goes across all taxonomic groups."


“…invasive species cost the British economy
  approximately £2bn a year…”

   “Invasive species are one of the greatest threats facing
        biodiversity today.”
                                              BBC News 13 October 2008
Plant Introductions
 - points of entry
Level of Plant
Invasion in
Europe
(% aliens)
 Chytry et al. (2009)
 Diversity & Distributions.
 15: 98-107
Plant Species in Britain & Ireland
              (after Preston et al. 2002)




 Total Number of Species              2711

 Native                               1363 (50.28%)

 Native/Alien*                              44 (1.62%)

 Naturalised Aliens*                  1304 (48.10%)


          * Species introduced after AD 1500
EVOLUTIONARY CONSEQUENCES
         OF INVASIONS
Invasives are models for studying

(i) Evolution in response to environmental change

(ii) Speciation and Gene transfer following
      hybridization with other species
Hybrid speciation
                  Species A       Species B


                              X
                     2n=10            2n=10

                 F1 hybrid

                              2n=10
                                                     Chromosome
                                                     doubling




         2n=10                                  2n=20

Homoploid hybrid species               Allopolyploid species
Origin of a new homoploid hybrid
  species - Senecio squalidus




  Oxford Ragwort (Senecio squalidus)
Oxford Ragwort (Senecio squalidus) in the UK
Brought to Oxford Botanic Gardens from Mount Etna, Sicily, 1700
               Escaped and spread around UK via railway network
The Senecio hybrid zone on
           Mount Etna, Sicily.
3000m




2000m
                                                   Senecio aethnensis



1000m
                                     Hybrid zone



 0m
        Senecio chrysanthemifolius
Morphological differences between
S. chrysanthemifolius and S. aethnensis




    Leaf shape and texture
    Flower head size
Differences between S. squalidus and its
               Sicilian relatives




 Intermediate morphology - distinct from wild
      hybrids on Mt. Etna
 Urban habitats: railways, walls, motorways
Surveyed RAPD variation for species diagnostic markers




Resolved:




              13 markers diagnostic of S. aethnensis
            2600 m




              13 markers diagnostic of S. chrysanthemifolius

            150 m
Ancestry of plants along     Ancestry of S. squalidus
altitude gradient, Mt Etna        plants in UK




            2600 m




                 150 m




                                       James JK, Abbott RJ (2005)
                                       Evolution 59: 2533-2547
Principal Coordinate Plot – RAPD Variation
PCo 2 (10.3%)




                                              PCo 1 (40.6%)

                      S. chrysanthemifolius   Hybrids   S. aethnensis   S. squalidus


                                                                           James JK, Abbott RJ (2005)
                                                                           Evolution 59: 2533-2547
HYBRID ORIGINS OF NEW TAXA IN SENECIO


S. aethnensis x S. chrysanthemifolius
   (2n=20)             (2n=20)

        S. squalidus
             (2n=20)

 1792
Introgression - Gene Transfer


         Species B                             Species A



                50% B   F1


                             25% B    Bc1


Movement of genes from
                                 12.5% B    Bc2
one species to another
by recurrent backcrossing
of hybrid to a parent                6.25% B      Bc3


                                     3.12% B       Bc4
Introgression (Gene transfer):

• Many examples based on analyses of neutral markers

• Very few examples involve genes affecting
      fitness

• Few examples where hybridizing species differ
      in ploidy and/or mating system
Hybridizes with native Groundsel (S. vulgaris)




  Oxford Ragwort (Senecio squalidus)
S. vulgaris               S. squalidus



Self-compatible               Self-incompatible




                     X


                     F1
                  (2n = 30)
                   sterile
   2n = 40                                2n =
                                          20
Effects of interspecific hybridization on gene expression
                                               10


          Normalised Expression (Log Scale)




                                              1.0




                                              0.1




                                                    S. squalidus   S. x baxteri   S. vulgaris


                                              S. squalidus               F1       S. vulgaris

‘Transcriptome shock’ in F1 hybrid. Normalized microarray expression data for
475 cDNA clones identified as showing significant differences in expression
between F1 and one or both progenitors. Hegarty et al. (2005) Molecular Ecology 14: 2493-2510
Hybrid evolution in Senecio
S. squalidus                                                        S. vulgaris
 Waste-sites,
 Roadsides,                            X                          Agricultural land
                                                                    Waste-sites,
   Walls                                                              Gardens

                      (2n=20)                     (2n=40)

                                  New Products




  S. cambrensis (2n=60)         S. eboracensis (2n=40)      Radiate S. vulgaris (2n=40)
  N.Wales & Edinburgh                Only in York              Widespread in UK
          1948                           1979                          1832
Radiate Groundsel (S. vulgaris var hibernicus )
Outcrossing rates of Non-Radiate (NN) and Radiate (RR)
                        plants




              Outcrossing rates

          Non-Radiate   Radiate

             1 - 15%     6 - 36%
Finding genes that produce ray florets


  • QTL analysis

  • Microarray analysis

  • Candidate gene approach √
Ray floret




Disc floret
CYCLOIDEA AS A CANDIDATE GENE




                                                         Snapdragon
                                                     (Antirrhinum majus)




   1 gene is largely responsible for change in
            flower shape: Cycloidea
            Encodes a transcription factor

               Luo et al. (1996) Nature 383: 794-9
               Luo et al. (1999) Cell 99: 367-76
• 6 cycloidea-like genes (RAY1-6) amplified in S. vulgaris

• 2 (RAY1 and RAY2) expressed in outer floret primordia
Semi-quantitative RT-PCR showing RAY1 and RAY2
expression in young flower heads of RR and NN S. vulgaris
RAY Cleaved Amplified Polymorphic Sequences (CAPS)




             Taq1 digest                   EcoR1 digest

• Linkage analysis: No recombinants for RAY1 or RAY2
        found among >700 F2 offspring of R/R x N/N cross

• Linkage confirmed by bulk segregant analysis of R/R
        and N/N genotypes: in each case no recombinants
        found among 2,800 chromosomes

• RAY1 and RAY2 are tightly linked and associated with RAY
DNA sequences of RAY1 and RAY2 genes
           associated with flower head forms




              N and N1 - Non-radiate sequences
              R and R1 - Radiate sequences

  Radiate S. vulgaris contains the R sequence found in S. squalidus

Confirms Radiate S. vulgaris received the R sequence from S. squalidus
Transformation studies
Do the RAY1 and RAY2 genes control development
     of ray florets in S. vulgaris flower head?
  • Developed transformation system for S. vulgaris
        using Agrobacterium tumefaciens strain GV3101
        and a Kanamycin resistance screen

  • Took sequences of RAY1 and RAY 2 genes from
         Non-radiate S. vulgaris (i.e. N alleles) and
         inserted them with 35S constitutive promoter
         into Radiate S. vulgaris
                       RAY1

                       RAY2
Transformants




     Control            *               *                 *                      ‡
* Expression of RAY1 N allele in Radiate S. vulgaris inhibits ray floret production
‡ Expression of RAY2 N allele in Radiate S. vulgaris produces tubular ray florets

  Both genes, RAY1 and RAY2, affect ray floret development

                                                     Kim et al. (2008) Science 322: 1116-1119
Conclusions

• We have isolated two genes RAY1 and RAY2 that control the
       development of ray florets in the flower heads of
       Senecio vulgaris

• Radiate alleles of RAY1 and RAY2 are tightly linked and were
        introgressed from the diploid S. squalidus to generate the
        radiate variant of S. vulgaris

 • Radiate S. vulgaris has a greater outcrossing rate than the
         non-radiate variant


 • This difference in outcrossing rate between the two morphs of
         S. vulgaris will affect their relative fitness in polymorphic
         populations
Maximum likelihood phylogeny of
                  RAY2 sequence variation

                      RAY2b-A
                                        Clade 1
                      RAY2b-C           (RAY2b)
                     RAY2b-B
                                  RAY2a-R
                                         RAY2a-N
                      100         100     RAY2a-Na
                                                                 Clade 2
                             68
                                          RAY2a-R2               (RAY2a)
                                   100       RAY2a-R2a
                             60            RAY2a-R1
                                    100     RAY2a-R1a
                      0.01




• Clades 1 and 2 represent two copies of RAY2 gene (RAY2a and RAY2b)

• Both copies are found in S. vulgaris (tetraploid). Diploids contain only RAY2a

                                                      Chapman & Abbott (2009) New Phytologist
Distribution of RAY2a-R
 and R1 alleles in S. squalidus




                       Aberdeen


                Edinburgh

                                        100%

                                        80%
                                                                                                          R
                                        60%
                       Leeds                                                                              R2
                                        40%
  Manchester                                                                                              R1
                                        20%
 Key:                  Birmingham
                                         0%
 R R1                                      NIC1    RAN1      MON1    SAP4    SAP2    SAP0    PRO2     ET3
           Oxford                         (755m)   (755m)   (1045m) (1364m) (1613m) (1915m) (2061m) (2287m)

                            Guildford

                                           Relative frequencies of RAY2a alleles in
                    Southampton             Senecio populations on Mount Etna
          Exmouth
                                                               Chapman & Abbott (2009) New Phytologist


Note: Only the ‘R’ allele has been introgressed into radiate S. vulgaris
HYBRID ORIGINS OF NEW TAXA IN SENECIO


S. aethnensis x S. chrysanthemifolius
   (2n=20)                   (2n=20)

        S. squalidus S. vulgaris
                   x                              S. eboracensis
             (2n=20)          (2n=40)                 (2n=40)
                                                                    1979
 1792
                       S. baxteri x S. vulgaris
                        (2n=30)         (2n=40)


                                          S. vulgaris (Radiate)
                 S. cambrensis              (2n=40)
                        (2n=60)                                   1832

        1948
Acknowledgements:

St Andrews University:   John Innes Centre:

      Mark Chapman             Rico Coen
      Amanda Gillies           Pilar Cubas
      Juliet James             Min-Long Cui
      Andy Lowe                Minsung Kim




                          Funded by NERC & BBSRC
The Environment Institute
                      Where ideas grow




   www.adelaide.edu.au/environment
   Phone: +61 8 8303 5379

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Plant Introductions & Evolution: Hybrid Speciation and Gene Transfer

  • 1. The Environment Institute Where ideas grow Richard Abbott Plant Introductions & Evolution: Hybrid Speciation and Gene Transfer
  • 2. Plant Introductions & Evolution: Hybrid Speciation and Gene Transfer Richard Abbott - St Andrews University, UK
  • 3. “There are almost 11,000 alien species in Europe and the trend of new arrivals is showing no signs of levelling out.” “…approximately 15% of the aliens within Europe are known to have some impact on the environment or economy - and this problem goes across all taxonomic groups." “…invasive species cost the British economy approximately £2bn a year…” “Invasive species are one of the greatest threats facing biodiversity today.” BBC News 13 October 2008
  • 4. Plant Introductions - points of entry
  • 5. Level of Plant Invasion in Europe (% aliens) Chytry et al. (2009) Diversity & Distributions. 15: 98-107
  • 6. Plant Species in Britain & Ireland (after Preston et al. 2002) Total Number of Species 2711 Native 1363 (50.28%) Native/Alien* 44 (1.62%) Naturalised Aliens* 1304 (48.10%) * Species introduced after AD 1500
  • 7. EVOLUTIONARY CONSEQUENCES OF INVASIONS Invasives are models for studying (i) Evolution in response to environmental change (ii) Speciation and Gene transfer following hybridization with other species
  • 8. Hybrid speciation Species A Species B X 2n=10 2n=10 F1 hybrid 2n=10 Chromosome doubling 2n=10 2n=20 Homoploid hybrid species Allopolyploid species
  • 9. Origin of a new homoploid hybrid species - Senecio squalidus Oxford Ragwort (Senecio squalidus)
  • 10. Oxford Ragwort (Senecio squalidus) in the UK Brought to Oxford Botanic Gardens from Mount Etna, Sicily, 1700 Escaped and spread around UK via railway network
  • 11. The Senecio hybrid zone on Mount Etna, Sicily. 3000m 2000m Senecio aethnensis 1000m Hybrid zone 0m Senecio chrysanthemifolius
  • 12. Morphological differences between S. chrysanthemifolius and S. aethnensis  Leaf shape and texture  Flower head size
  • 13. Differences between S. squalidus and its Sicilian relatives  Intermediate morphology - distinct from wild hybrids on Mt. Etna  Urban habitats: railways, walls, motorways
  • 14. Surveyed RAPD variation for species diagnostic markers Resolved: 13 markers diagnostic of S. aethnensis 2600 m 13 markers diagnostic of S. chrysanthemifolius 150 m
  • 15. Ancestry of plants along Ancestry of S. squalidus altitude gradient, Mt Etna plants in UK 2600 m 150 m James JK, Abbott RJ (2005) Evolution 59: 2533-2547
  • 16. Principal Coordinate Plot – RAPD Variation PCo 2 (10.3%) PCo 1 (40.6%) S. chrysanthemifolius Hybrids S. aethnensis S. squalidus James JK, Abbott RJ (2005) Evolution 59: 2533-2547
  • 17. HYBRID ORIGINS OF NEW TAXA IN SENECIO S. aethnensis x S. chrysanthemifolius (2n=20) (2n=20) S. squalidus (2n=20) 1792
  • 18. Introgression - Gene Transfer Species B Species A 50% B F1 25% B Bc1 Movement of genes from 12.5% B Bc2 one species to another by recurrent backcrossing of hybrid to a parent 6.25% B Bc3 3.12% B Bc4
  • 19. Introgression (Gene transfer): • Many examples based on analyses of neutral markers • Very few examples involve genes affecting fitness • Few examples where hybridizing species differ in ploidy and/or mating system
  • 20. Hybridizes with native Groundsel (S. vulgaris) Oxford Ragwort (Senecio squalidus)
  • 21. S. vulgaris S. squalidus Self-compatible Self-incompatible X F1 (2n = 30) sterile 2n = 40 2n = 20
  • 22. Effects of interspecific hybridization on gene expression 10 Normalised Expression (Log Scale) 1.0 0.1 S. squalidus S. x baxteri S. vulgaris S. squalidus F1 S. vulgaris ‘Transcriptome shock’ in F1 hybrid. Normalized microarray expression data for 475 cDNA clones identified as showing significant differences in expression between F1 and one or both progenitors. Hegarty et al. (2005) Molecular Ecology 14: 2493-2510
  • 23. Hybrid evolution in Senecio S. squalidus S. vulgaris Waste-sites, Roadsides, X Agricultural land Waste-sites, Walls Gardens (2n=20) (2n=40) New Products S. cambrensis (2n=60) S. eboracensis (2n=40) Radiate S. vulgaris (2n=40) N.Wales & Edinburgh Only in York Widespread in UK 1948 1979 1832
  • 24. Radiate Groundsel (S. vulgaris var hibernicus )
  • 25. Outcrossing rates of Non-Radiate (NN) and Radiate (RR) plants Outcrossing rates Non-Radiate Radiate 1 - 15% 6 - 36%
  • 26. Finding genes that produce ray florets • QTL analysis • Microarray analysis • Candidate gene approach √
  • 28. CYCLOIDEA AS A CANDIDATE GENE Snapdragon (Antirrhinum majus) 1 gene is largely responsible for change in flower shape: Cycloidea Encodes a transcription factor Luo et al. (1996) Nature 383: 794-9 Luo et al. (1999) Cell 99: 367-76
  • 29. • 6 cycloidea-like genes (RAY1-6) amplified in S. vulgaris • 2 (RAY1 and RAY2) expressed in outer floret primordia
  • 30.
  • 31. Semi-quantitative RT-PCR showing RAY1 and RAY2 expression in young flower heads of RR and NN S. vulgaris
  • 32. RAY Cleaved Amplified Polymorphic Sequences (CAPS) Taq1 digest EcoR1 digest • Linkage analysis: No recombinants for RAY1 or RAY2 found among >700 F2 offspring of R/R x N/N cross • Linkage confirmed by bulk segregant analysis of R/R and N/N genotypes: in each case no recombinants found among 2,800 chromosomes • RAY1 and RAY2 are tightly linked and associated with RAY
  • 33. DNA sequences of RAY1 and RAY2 genes associated with flower head forms N and N1 - Non-radiate sequences R and R1 - Radiate sequences Radiate S. vulgaris contains the R sequence found in S. squalidus Confirms Radiate S. vulgaris received the R sequence from S. squalidus
  • 34. Transformation studies Do the RAY1 and RAY2 genes control development of ray florets in S. vulgaris flower head? • Developed transformation system for S. vulgaris using Agrobacterium tumefaciens strain GV3101 and a Kanamycin resistance screen • Took sequences of RAY1 and RAY 2 genes from Non-radiate S. vulgaris (i.e. N alleles) and inserted them with 35S constitutive promoter into Radiate S. vulgaris RAY1 RAY2
  • 35. Transformants Control * * * ‡ * Expression of RAY1 N allele in Radiate S. vulgaris inhibits ray floret production ‡ Expression of RAY2 N allele in Radiate S. vulgaris produces tubular ray florets Both genes, RAY1 and RAY2, affect ray floret development Kim et al. (2008) Science 322: 1116-1119
  • 36. Conclusions • We have isolated two genes RAY1 and RAY2 that control the development of ray florets in the flower heads of Senecio vulgaris • Radiate alleles of RAY1 and RAY2 are tightly linked and were introgressed from the diploid S. squalidus to generate the radiate variant of S. vulgaris • Radiate S. vulgaris has a greater outcrossing rate than the non-radiate variant • This difference in outcrossing rate between the two morphs of S. vulgaris will affect their relative fitness in polymorphic populations
  • 37. Maximum likelihood phylogeny of RAY2 sequence variation RAY2b-A Clade 1 RAY2b-C (RAY2b) RAY2b-B RAY2a-R RAY2a-N 100 100 RAY2a-Na Clade 2 68 RAY2a-R2 (RAY2a) 100 RAY2a-R2a 60 RAY2a-R1 100 RAY2a-R1a 0.01 • Clades 1 and 2 represent two copies of RAY2 gene (RAY2a and RAY2b) • Both copies are found in S. vulgaris (tetraploid). Diploids contain only RAY2a Chapman & Abbott (2009) New Phytologist
  • 38. Distribution of RAY2a-R and R1 alleles in S. squalidus Aberdeen Edinburgh 100% 80% R 60% Leeds R2 40% Manchester R1 20% Key: Birmingham 0% R R1 NIC1 RAN1 MON1 SAP4 SAP2 SAP0 PRO2 ET3 Oxford (755m) (755m) (1045m) (1364m) (1613m) (1915m) (2061m) (2287m) Guildford Relative frequencies of RAY2a alleles in Southampton Senecio populations on Mount Etna Exmouth Chapman & Abbott (2009) New Phytologist Note: Only the ‘R’ allele has been introgressed into radiate S. vulgaris
  • 39. HYBRID ORIGINS OF NEW TAXA IN SENECIO S. aethnensis x S. chrysanthemifolius (2n=20) (2n=20) S. squalidus S. vulgaris x S. eboracensis (2n=20) (2n=40) (2n=40) 1979 1792 S. baxteri x S. vulgaris (2n=30) (2n=40) S. vulgaris (Radiate) S. cambrensis (2n=40) (2n=60) 1832 1948
  • 40. Acknowledgements: St Andrews University: John Innes Centre: Mark Chapman Rico Coen Amanda Gillies Pilar Cubas Juliet James Min-Long Cui Andy Lowe Minsung Kim Funded by NERC & BBSRC
  • 41. The Environment Institute Where ideas grow www.adelaide.edu.au/environment Phone: +61 8 8303 5379