The advantages and
disadvantages of being polyploid
Luca Comai
Nature Publishing Group
November 2005
The advantages and disadvantages of
being polyploid
•
•
•
•
•
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Polyploidy
The mechanics of polyploidy
Advantages of polyploidy
Disadvantages of polyploidy
Evolutionary potential of polyploids
Outlook
Polyploidy
• 倍数性：近縁の種・品種などの間において、染色体数に
増減の見られる現象
• Ｈ．ヴィンクラー（１９１６）提唱
• 基本数の完全な整数倍のときを正倍数性（euploidy）、
不完全なときを異数性（aneuploidy）という
• 植物では倍数体の人為的な作成がたやすく、切断法・温
度処理法などがあり、特にコルヒチン処理は育種に多用
されている
The mechanics of polyploidy
•
Formation and incidence of polyploidy
– Polyploids arise when a rare mitotic or meiotic catastrophe causes the
formation of gametes that have more than one set of chromosomes.
– Autopolyploids are of the same type and have the same origin
– Allopolyploids both the type and the origin are different
•
Polyploids form at relatively high frequency (1 per 100,000) in flowering
plants.
•
Higher vertebrates do not tolerate polyploidy, but 10% of spontaneous
abortions in humans are due to polyploidy.
Figure 1
Evolutionary alternation of diploidy and polyploidy.
The possible paths that result in the sudden
transition from diploidy to polyploidy
and the gradual transition from
polyploidy to diploidy.
Polyploids arisen when a rare mitotic or
meiotic catastrophe causes the
formation of gametes that have more
than one set of choromosomes.
Figure 2-a,b
Polyploid formation and ensuing meiotic irregularities.
•
Meiotic pairing arrangements
vary between ploidy types.
•
The pairing of homologous
chromosomes is defective in the
F1 hybrid because of
divergence in the structure and
number of chromosomes.
Figure 2-c
Polyploid formation and ensuing mitotic irregularities.
In animal cells, the centrosome number response in genome
size by forming multiple spindles that result in unbalanced
mitotic products.
Centrosome：中心体
動物細胞や下等植物細胞の細胞小器官
Figure 3
Contrasting patterns of inheritance in diplods and polyploids.
•
A diploid heterozygote Aa
produces two types of gamete
in equal proporion.
•
An autotetrapolyploid with
genotype AAaa produces three
types of gamete.
•
An allotetraploid with genotype
AaAa produces four types of
gamete.
Advantages of polypoloidy
• Heterosis
• Gene redundancy
• Loss of self-incompatibility and gain of asexual
reproduction
Heterosis (hybrid vigor)
•
雑種強勢：生物の雑種第一代がある形質、例えば大きさ・耐性・収
量・多産性などの点で、両親の系統のいずれをも凌ぐこと
– 対立遺伝子の相互作用があり、ヘテロはホモより問題の形質について
優れている
– 両親に含まれていた異なる優性遺伝子が雑種第一代において共存する
こと（優性遺伝子がこれに対応する劣性遺伝子よりも問題の形質につい
て優れていおり、雑種では劣性遺伝子の効果が覆い隠されることによ
る）
Inbreeding depression
•
近交弱勢：近親交配を長く続けることにより、大きさ・耐性・多産性な
ど、一般に生活力が低下する現象
– ホモ接合の遺伝子座が増加し、劣勢有害遺伝子の影響や雑種強勢に
関わる遺伝子の喪失が原因となる
– 動物や他家受精植物においてとくに顕著であるが、弱勢の程度は種類
や系統によってかなり違う
Heterosis (hybrid vigor)
• The fixing of divergent parental genomes in allopolyploids.
• Heterosis can be exploited at the 1N (haploid) stages of
polyploid plants and also in animals.
• Autopolyploid hybrids show stronger heterosis than the
corresponding diploid hybrids
• Autopolyploid inbreds show stronger inbreeding
depression than diploid inbreds.
Gene redundancy
• The masking of recessive alleles by dominant wild-type
alleles.
– The gametophytic, haploid stage
– 2N phase, polyploidy can reduce the incidence of homozygous
recessives
• The ability to diversify gene function by altering redundant
copies of important or essential genes.
Figure 3
Contrasting patterns of inheritance in diplods and polyploids.
•
A diploid heterozygote Aa
produces 1/4 aa homozygotes.
•
An autotetrapolyploid with
genotype AAaa produces
1/36aaaa homozygotes.
•
An allotetraploid with genotype
AaAa produces 1/16aaaa
homozygotes.
Gene redundancy
• The masking of recessive alleles by dominant wild-type
alleles.
– The gametophytic, haploid stage
– 2N phase, polyploidy can reduce the incidence of homozygous
recessives
• The ability to diversify gene function by altering redundant
copies of important or essential genes.
– In diploids, such an ability is conditional on the occurrence of a
rare segmental duplication event.
– In polyploids, all genes have a duplicated copy that is available for
evolutionary experimentation.
Loss of self-incompatibility and gain of
asexual reproduction
• Polyploidy can affect sexuality.
• By disrupting certain self-incompatibility
systems, allowing self-fertilization
– The molecular basis of this response is unclear.
• In allopolyploids, A.thaliana, it might result from
interactions between the parental genomes.
• In autopolyploid, Petunia hybrida, it could result
from interallelic interactions in the 2X pollen.
• By favoring the onset of asexual
reproduction, which is associated with
polyploidy in both animals and plants.
Polyploidy and sexuality
• Polyploiy is associated with the formation of apomictic
species.
• Genes for apomixis might
– be linked to recessive lethals.
– be linked to loci that aresubject to segregation distortion in haplod
gametes.
– be located on chromosomes that are ineffcient at pairing.
Polyploidy might facilitate the spread of a species
by avoiding the need for sexual mates.
Segregation distortion
• 分離の歪み：メンデル遺伝において、期待される分離比
が得られないこと、分離の法則に従わない現象
– メンデル遺伝では、接合体中の相同遺伝子は配偶子に均等に
分配されるが、この公平さをごまかす遺伝子があり、メンデル遺
伝の歪みとして現れる
– 最もよく知られた例はキイロショウジョウバエのＳＤ因子であり、
他にもマウスのt遺伝子をはじめ、カ・バッタ、植物ではトウモロコ
シ・タバコでも類似の遺伝子が存在する
Advantages of polypoloidy
• Heterosis
– The ability to make better use of heterozygosity
• Gene redundancy
– The buffering effect of gene redundancy on mutations
• Loss of self-incompatibility and gain of asexual reproduction
– The facilitation of reproduction through self-fertilization or asexual
means.
Disadvantages of polyploidy
•
•
•
•
•
Changes in cellular architecture, and regulatory implications.
Difficulties in mitosis.
Difficulties in meiosis.
Regulatory changes in gene expression.
Epigenetic instability.
– autopolyploids
– allopolyploids
Changes in cellular architecture, and
regulatory implications.
• Increasing the genomic content of an organism usually
increase cell volume, with a consequent change in the
relationship between the three-dimensional and dimensional
components of the cell.
• An increase in the amount of DNA and, in the cell volume can
be advantageous for cells that have high metabolic rate.
– Most organisms can modulate the amount of DNA in their nucleus by
undergoing DNA endoreduplication, which leads to endopolyploid
cells.
Endopolyploidy
•
Having a genome content that is
greater than the germ line and
which usually results from
cycles of DNA replication in
the absence of mitosis.
•
Difference between polyploidy
and endopolyploidy
– Heterochromatin
– The genetic make up of cells
The endoreduplicated state of
diploid cells is not directly
equivalent to true polyploid.
Difficulties in mitosis.
• Difficulties in mitosis can arise from spindle irregularities.
• There is little information on the mitotic stability of polyploid
plant cells.
• Although the susceptibility of autopolyploids to the mitotic
production of aneuploids might vary from taxon to taxon, the
available data indicate the existence of a considerable risk of
aneuploidy.
Difficulties in meiosis.
• Autopolyploids
– Autopolyploids have the potential to form multivalents
at meiotic metaphase I.
– A tetravalent can produce abnormal segregation
patterns such as ‘3:1’or ‘2:1 plus one laggard’.
Difficulties in meiosis.
• Autopolyploids
– In triploids, trivalents cannot be resolved into balanced
products.
– Random segregation of multiple chromosome types
produces mostly aneuploid gametes.
– Depending on the species, aneuploid gametes and
resulting zygotes vary in viability.
Viability of gametes and zygotes arising from
autotriploids and autopentaploids
• The aneuploid gametes and resulting zygotes vary in
viability.
– Triploid hybrid watermelon(seedless)
– Spinach and A.thaliana(fertile)
• This degree of fertility and the ability to produce progeny
of different ploidy serve as
– Intermediates in the formation of tetraploids
– Gene conduits between diploids and tetraploids
• It is not known what causes different triploid species to
vary in fertility and in tolerance to aneuploidy.
Difficulties in meiosis.
• Aneuploid gametes can be produced by polyploid meiosis,
although their frequency varies between species and
according to polyploidy types.
• There is a casual relationship between polyploidy and
aneuploidy.
• Eupolyploids produce frequent aneuploids, which can
produce euploids.
• Aneuploidy can cause epigenetic changes.
Regulatory changes in gene expression.
• Changes in gene expression
– are thought to be deleterious
– are likely to contribute to heterosis
– can provide variation that might allow adaptation to novel
conditions
• An increase in the copy number of all chromosomes affect
all genes equally and should result in a uniform increase in
gene expression.
• Polyploidy changes the structural relationship between
certain cellular components and alter the progress of
mitosis and meiosis.
Regulatory changes in gene expression.
• The first study of the effects of ploidy measured the
mRNA levels per genome for 18 genes in 1X, 2X, 3X and
4X maize.
– the odd-ploidy response
– B chromosomes
B chromosome
•
B-染色体：１組の基本染色体（A染色体）のほかに、余分に含まれる染
色体または染色体断片
– 通常の染色体をA染色体と呼ぶのに対する用語
– 数と大きさは多様
– 一般に端部に動原体を持つもの、異質染色質を比較的多く含むものが多い
– 減数分裂ではA染色体とは相同的に対合せず、またB染色体どうしの対合
力も非常に弱い
– 個体間で数と形の変異が著しく、同一個体内の細胞でも数が変わることもあ
る
– B染色体の多くは遺伝的に不活性であるが、その数が多くなると稔性が低
下する
– 植物ではトウモロコシ・ライムギなど、動物ではバタ・ネズミ・タヌキなどでそ
の存在が知られている
Regulatory changes in gene expression.
• the mRNA levels per genome for 18 genes in 1X, 2X, 3X
and 4X maize.
– the odd-ploidy response
– B chromosomes
• Saccharomyces cerevisiae in 1X, 2X, 3X and 4X cells.
Regulatory changes in gene expression.
• The consequence of autopolyploidization on gene
expression have not been sufficiently clarified in animals
or plants.
• A relatively small fraction of plant genes should have
measurable changes in diploid-tetraploid comparison, and
another fraction should response to odd-ploidy.
• It will be important to compare genotypically matched
diploid, triploid and tetraploid individuals and to rule out
spurious effects.
Epigenetic
• 後成的：
– 遺伝子の作用に直接関係なしに起こる発生における
変化
– 遺伝子が他の同じ細胞間で遺伝子活性の調節機構
の違いによって起こる分化
– DNA配列の変化ではなく、DNAの共有結合やヒスト
ンのようなクロマチンタンパクの修飾による遺伝子発
現における安定した変化
Epigenetic instability.
• Autopolyploids
– The epigenetic effects at a transgenic locus were compared
between diploid and tetraploid A.thaliana.(Figure 4)
– The standard Columbia accession Col-0
– The Zurich accession
• It could not be ruled out that autopolyploidization had
caused a genomic shock that changed the epigenetic
regulation of random targets.
Figure4
Ploidy-dependent paramutation.
(based on the assumption that the conversion from the active
to inactive state occurs during meiosis)
•
•
•
A polyploidy-dependent ability to
convert an active locus to an inactive
one.
The same locus was incapable of
affecting the active allele in diploid.
A tetraploid heterozygote(RRrr)
produced gametes that were
predominantly r, violating the
Mendelian rule of allelic segregation.
Epigenetic instability.
• Allopolyploids
– Structural genomic and expression changes to DNA methylation
changes have been done in A.thaliana and wheat.
• In A.thaliana, neoallopolyploids were produced by crossing
two autotetraploid parents
• In wheat, by crossing diploid parents and duplicating the
chromosomes of F1 hybrids.
The instability syndrome of neoallopolyploids should be
attributed to parental regulatory divergence and
intergenomic incompatibilities.
Epigenetic instability.
• Another possible cause of epigenetic remodeling is
aneuploidy.
– By altering the dosage of factors
– Through the exposure of unpaired chromatin regions
• Once a chromosomal region has become imprinted it
would be inherited stably even when the cause of
imprinting is removed.
Some of the epigenetic instability that is observed in
polyploids might result from aneuploidy.
Evolutionary potential of polyploids
•
•
What is the effect of the widespread epigenetic changes?
– Seem to be deleterious
– Contribute to the adaptive potential of polyploids
• Increasing heterosis
• Increasing diversity and plasticity
A fertility barrier must be overcome to take advantage of the adaptive
traits that are conferred by allopolyploiy.
It is not known whether regulatory changes reflect a preferential
interaction of normal, cell-specific regulatory factors or whether tissuespecific epigenetic regulation.
Outlook
• Selective pressures act immediately after polyploidization
and have protracted effects, so elucidating them is
important to understanding the evolution of polyploids.
• We still need to understand the different regulatory
consequences of autopolyploidy versus allopolyploidy and
the effect of aneuploidy on polyploids.
• We need to identify which adaptations might facilitate the
transition from diploidy to polyploidy.