Paleopolyploidy

Image:PaleopolyploidyTree.jpg

Ancient genome duplications are widespread throughout eukaryotic lineages, particularly in plants. Studies suggest that the common ancestor of Poaceae, the grass family which includes important crop species such as maize, rice, wheat, and sugar cane, shared a whole genome duplication about {{ma|70}}.{{cite journal | vauthors = Paterson AH, Bowers JE, Chapman BA | title = Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 101 | issue = 26 | pages = 9903–8 | date = June 2004 | pmid = 15161969 | pmc = 470771 | doi = 10.1073/pnas.0307901101 | bibcode = 2004PNAS..101.9903P | doi-access = free }} In more ancient monocot lineages one or likely multiple rounds of additional whole genome duplications had occurred, which were however not shared with the ancestral eudicots.{{cite journal | vauthors = Tang H, Bowers JE, Wang X, Paterson AH | title = Angiosperm genome comparisons reveal early polyploidy in the monocot lineage | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 107 | issue = 1 | pages = 472–7 | date = January 2010 | pmid = 19966307 | pmc = 2806719 | doi = 10.1073/pnas.0908007107 | bibcode = 2010PNAS..107..472T | doi-access = free }} Further independent more recent whole genome duplications have occurred in the lineages leading to maize, sugar cane and wheat, but not rice, sorghum or foxtail millet.{{Cn|date=January 2021}}

A polyploidy event {{ma|160}} is theorized to have created the ancestral line that led to all modern flowering plants.{{cite journal | vauthors = Callaway E | title = Shrub genome reveals secrets of flower power | journal = Nature |date=December 2013 | doi = 10.1038/nature.2013.14426 | url = http://www.nature.com/news/shrub-genome-reveals-secrets-of-flower-power-1.14426?WT.mc_id=GPL_NatureNews | s2cid = 88293665 }} That paleopolyploidy event was studied by sequencing the genome of an ancient flowering plant, Amborella trichopoda.{{cite journal | vauthors = Adams K | title = Genomics. Genomic clues to the ancestral flowering plant | journal = Science | volume = 342 | issue = 6165 | pages = 1456–7 | date = December 2013 | pmid = 24357306 | doi = 10.1126/science.1248709 | bibcode = 2013Sci...342.1456A | s2cid = 206553839 }}

The core eudicots also shared a common whole genome triplication (paleo-hexaploidy), which was estimated to have occurred after monocot-eudicot divergence but before the divergence of rosids and asterids.{{cite journal | vauthors = Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH | title = Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps | journal = Genome Research | volume = 18 | issue = 12 | pages = 1944–54 | date = December 2008 | pmid = 18832442 | pmc = 2593578 | doi = 10.1101/gr.080978.108 }}{{cite journal | vauthors = Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P | display-authors = 6 | title = The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla | journal = Nature | volume = 449 | issue = 7161 | pages = 463–7 | date = September 2007 | pmid = 17721507 | doi = 10.1038/nature06148 | bibcode = 2007Natur.449..463J | doi-access = free | hdl = 11577/2430527 | hdl-access = free }}{{cite journal | vauthors = Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH | title = Synteny and collinearity in plant genomes | journal = Science | volume = 320 | issue = 5875 | pages = 486–8 | date = April 2008 | pmid = 18436778 | doi = 10.1126/science.1153917 | bibcode = 2008Sci...320..486T | s2cid = 206510918 }} Many eudicot species have experienced additional whole genome duplications or triplications. For example, the model plant Arabidopsis thaliana, the first plant to have its entire genome sequenced, has experienced at least two additional rounds of whole genome duplication since the duplication shared by the core eudicots.{{cite journal | vauthors = Bowers JE, Chapman BA, Rong J, Paterson AH | title = Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events | journal = Nature | volume = 422 | issue = 6930 | pages = 433–8 | date = March 2003 | pmid = 12660784 | doi = 10.1038/nature01521 | bibcode = 2003Natur.422..433B | s2cid = 4423658 }} The most recent event took place before the divergence of the Arabidopsis and Brassica lineages, about {{ma|20}} to {{ma|45}}. Other examples include the sequenced eudicot genomes of apple, soybean, tomato, cotton, etc.{{Cn|date=January 2021}}

Compared with plants, paleopolyploidy is much rarer in the animal kingdom. It has been identified mainly in amphibians and bony fishes. Although some studies suggested one or more common genome duplications are shared by all vertebrates (including humans), the evidence is not as strong as in the other cases because the duplications, if they exist, happened so long ago (about 400-500 Ma compared to less than 200 Ma in plants), and the matter is still under debate. The idea that vertebrates share a common whole genome duplication is known as the 2R Hypothesis. Many researchers are interested in the reason why animal lineages, particularly mammals, have had so many fewer whole genome duplications than plant lineages.{{Cn|date=January 2021}}

A well-supported paleopolyploidy has been found in baker's yeast (Saccharomyces cerevisiae), despite its small, compact genome (~13Mbp), after the divergence from Kluyveromyces lactis and K. marxianus.{{cite journal | vauthors = Wong S, Butler G, Wolfe KH | title = Gene order evolution and paleopolyploidy in hemiascomycete yeasts | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 99 | issue = 14 | pages = 9272–7 | date = July 2002 | pmid = 12093907 | pmc = 123130 | doi = 10.1073/pnas.142101099 | bibcode = 2002PNAS...99.9272W | author-link3 = Kenneth H. Wolfe | doi-access = free }} Through genome streamlining, yeast has lost 90% of the duplicated genome over evolutionary time and is now recognized as a diploid organism.{{Cn|date=January 2021}}

{{Unreferenced section|date=January 2021}}

Duplicated genes can be identified through sequence homology on the DNA or protein level. Paleopolyploidy can be identified as massive gene duplication at one time using a molecular clock. To distinguish between whole-genome duplication and a collection of (more common) single gene duplication events, the following rules are often applied:

Image:NumbervsKs.jpg

• Duplicated genes are located in large duplicated blocks. Single gene duplication is a random process and tends to make duplicated genes scattered throughout the genome.
• Duplicated blocks are non-overlapping because they were created simultaneously. Segmental duplication within the genome can fulfill the first rule; but multiple independent segmental duplications could overlap each other.{{Cite journal |last1=Flagel |first1=Lex E. |last2=Wendel |first2=Jonathan F. |date=2009 |title=Gene duplication and evolutionary novelty in plants |url=https://nph.onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2009.02923.x |journal=New Phytologist |language=en |volume=183 |issue=3 |pages=557–564 |doi=10.1111/j.1469-8137.2009.02923.x |pmid=19555435 |issn=1469-8137}}

In theory, the two duplicated genes should have the same "age"; that is, the divergence of the sequence should be equal between the two genes duplicated by paleopolyploidy (homeologs). Synonymous substitution rate, Ks, is often used as a molecular clock to determine the time of gene duplication.{{Cite journal |last=Eckardt |first=Nancy A. |date=July 2004 |title=Two Genomes Are Better Than One: Widespread Paleopolyploidy in Plants and Evolutionary Effects |journal=The Plant Cell |language=en |volume=16 |issue=7 |pages=1647–1649 |doi=10.1105/tpc.160710 |pmid=15272471 |pmc=514149 |issn=1040-4651 }} Thus, paleopolyploidy is identified as a "peak" on the duplicate number vs. Ks graph (shown on the right).

However, using Ks plots to identify and document ancient polyploid events can be problematic, as the method fails to identify genome duplications that were followed by massive gene elimination and genome refinement. Other mixed model approaches that combined Ks plots with other methods are being developed to better understand paleopolyploidy.{{cite journal | vauthors = Tiley GP, Barker MS, Burleigh JG | title = Assessing the Performance of Ks Plots for Detecting Ancient Whole Genome Duplications | journal = Genome Biology and Evolution | volume = 10 | issue = 11 | pages = 2882–2898 | date = November 2018 | pmid = 30239709 | pmc = 6225891 | doi = 10.1093/gbe/evy200 }}

Duplication events that occurred a long time ago in the history of various evolutionary lineages can be difficult to detect because of subsequent diploidization (such that a polyploid starts to behave cytogenetically as a diploid over time) as mutations and gene translations gradually make one copy of each chromosome unlike its counterpart. This usually results in a low confidence for identifying ancient paleopolyploidy.{{Cite journal |last1=Campbell |first1=Matthew A. |last2=Ganley |first2=Austen R. D. |last3=Gabaldón |first3=Toni |last4=Cox |first4=Murray P. |date=December 2016 |title=The Case of the Missing Ancient Fungal Polyploids |url=https://www.journals.uchicago.edu/doi/full/10.1086/688763#_i10 |journal=The American Naturalist |volume=188 |issue=6 |pages=602–614 |doi=10.1086/688763 |issn=0003-0147}}

Paleopolyploidization events lead to massive cellular changes, including doubling of the genetic material, changes in gene expression and increased cell size. Gene loss during diploidization is not completely random, but heavily selected. Genes from large gene families are duplicated. On the other hand, individual genes are not duplicated.{{clarify|date=February 2018}} Overall, paleopolyploidy can have both short-term and long-term evolutionary effects on an organism's fitness in the natural environment.{{Cn|date=January 2021}}

Whole genome duplication may increase the rates and efficiency by which organisms acquire new biological traits. However, one test of this hypothesis, which compared evolutionary rates in innovation in early teleost fishes (with duplicate genomes) to early holostean fishes (without duplicated genomes) found little difference between the two.

Genome doubling provided the organism with redundant alleles that can evolve freely with little selection pressure. The duplicated genes can undergo neofunctionalization, subfunctionalization, or nonfunctionalization which could help the organism adapt to the new environment or survive different stress conditions.{{Cite journal |last1=Akagi |first1=Takashi |last2=Jung |first2=Katharina |last3=Masuda |first3=Kanae |last4=Shimizu |first4=Kentaro K. |date=2022-10-01 |title=Polyploidy before and after domestication of crop species |url=https://www.sciencedirect.com/science/article/pii/S136952662200084X#:~:text=After%20polyploidization,%20duplicated%20gene%20pairs%20often%20undergo,redundancy%20or%20adaptive%20conflicts%20%5B11,%2012,%2013%5D.&text=Interestingly,%20this%20subfunctionalization%20is%20similar%20in%20natural,alteration%20may%20have%20been%20evolutionarily%20stable%20%5B50,51%5D. |journal=Current Opinion in Plant Biology |volume=69 |pages=102255 |doi=10.1016/j.pbi.2022.102255 |pmid=35870416 |issn=1369-5266}}

Polyploids often have larger cells and even larger organs. Many important crops, including wheat, maize and cotton, are paleopolyploids which were selected for domestication by ancient peoples.{{Cite journal |last=Chen |first=Z Jeffrey |date=February 2010 |title=Molecular mechanisms of polyploidy and hybrid vigor |journal=Trends in Plant Science |volume=15 |issue=2 |pages=57–71 |doi=10.1016/j.tplants.2009.12.003 |pmid=20080432 |pmc=2821985 }}

It has been suggested that many polyploidization events created new species, via a gain of adaptive traits, or by sexual incompatibility with their diploid counterparts. An example would be the recent speciation of allopolyploid Spartina — S. anglica; the polyploid plant is so successful that it is listed as an invasive species in many regions.{{cite journal | vauthors = te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubesová M, Pysek P | title = The more the better? The role of polyploidy in facilitating plant invasions | journal = Annals of Botany | volume = 109 | issue = 1 | pages = 19–45 | date = January 2012 | pmid = 22040744 | pmc = 3241594 | doi = 10.1093/aob/mcr277 }}

There are two major divisions of polyploidy, allopolyploidy and autopolyploidy. Allopolyploids arise as a result of the hybridization of two related species, while autopolyploids arise from the duplication of a species' genome as a result of hybridization of two conspecific parents,{{cite journal | vauthors = Soltis PS, Soltis DE | title = The role of genetic and genomic attributes in the success of polyploids | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 97 | issue = 13 | pages = 7051–7 | date = June 2000 | pmid = 10860970 | pmc = 34383 | doi = 10.1073/pnas.97.13.7051 | author-link = Pamela S. Soltis | bibcode = 2000PNAS...97.7051S | doi-access = free }} or somatic doubling in reproductive tissue of a parent. Allopolyploid species are believed to be much more prevalent in nature, possibly because allopolyploids inherit different genomes, resulting in increased heterozygosity, and therefore higher fitness. These different genomes result in an increased likelihood of large genomic reorganizations,{{cite journal | vauthors = Parisod C, Holderegger R, Brochmann C | title = Evolutionary consequences of autopolyploidy | journal = The New Phytologist | volume = 186 | issue = 1 | pages = 5–17 | date = April 2010 | pmid = 20070540 | doi = 10.1111/j.1469-8137.2009.03142.x | doi-access = }} which can be either deleterious, or advantageous. Autopolyploidy, however, is generally considered to be a neutral process, though it has been hypothesized that autopolyploidy may serve as a useful mechanism for inducing speciation, and therefore assisting in the ability of an organism to quickly colonize in new habitats without undergoing the time-intensive and costly period of genomic reorganization experienced by allopolyploid species. One common source of autopolyploidy in plants stems from "perfect flowers", which are capable of self-pollination, or "selfing". This, along with errors in meiosis that lead to aneuploidy, can create an environment where autopolyploidy is very likely. This fact can be exploited in a laboratory setting by using colchicine to inhibit chromosome segregation during meiosis, creating synthetic autopolyploid plants.{{Cite journal |last1=Manzoor |first1=Ayesha |last2=Ahmad |first2=Touqeer |last3=Bashir |first3=Muhammad Ajmal |last4=Hafiz |first4=Ishfaq Ahmad |last5=Silvestri |first5=Cristian |date=July 2019 |title=Studies on Colchicine Induced Chromosome Doubling for Enhancement of Quality Traits in Ornamental Plants |journal=Plants |language=en |volume=8 |issue=7 |pages=194 |doi=10.3390/plants8070194 |doi-access=free |pmid=31261798 |pmc=6681243 |issn=2223-7747}}

Following polyploidy events, there are several possible fates for duplicated genes; both copies may be retained as functional genes, change in gene function may occur in one or both copies, gene silencing may mask one or both copies, or complete gene loss may occur.{{cite book |author=Wendel JF |title=Plant Molecular Evolution |chapter=Genome evolution in polyploids |journal=Plant Molecular Biology |volume=42 |pages=225–249 |date=2000 |issue=1 | doi = 10.1007/978-94-011-4221-2_12 |pmid=10688139 |isbn=978-94-010-5833-9 }} Polyploidy events will result in higher levels of heterozygosity, and, over time, can lead to an increase in the total number of functional genes in the genome. As time passes after a genome duplication event, many genes will change function as a result of either change in duplicate gene function for both allo- and autopolyploid species, or there will be changes in gene expression caused by genomic rearrangements induced by genome duplication in allopolyploids. When both copies of a gene are retained, and thus the number of copies doubled, there is a chance that there will be a proportional increase in expression of that gene, resulting in twice as much mRNA transcript being produced. There is also the possibility that transcription of a duplicated gene will be down-regulated, resulting in less than two-fold increase in transcription of that gene, or that the duplication event will yield more than a two-fold increase in transcription.{{cite journal | vauthors = Coate JE, Doyle JJ | title = Quantifying whole transcriptome size, a prerequisite for understanding transcriptome evolution across species: an example from a plant allopolyploid | journal = Genome Biology and Evolution | volume = 2 | pages = 534–46 | date = 2010 | pmid = 20671102 | pmc = 2997557 | doi = 10.1093/gbe/evq038 }} In one species, Glycine dolichocarpa (a close relative of the soybean, Glycine max), it has been observed that following a genome duplication roughly 500,000 years ago, there has been a 1.4 fold increase in transcription, indicating that there has been a proportional decrease in transcription relative to gene copy number following the duplication event.

The hypothesis of vertebrate paleopolyploidy originated as early as the 1970s, proposed by the biologist Susumu Ohno. He reasoned that the vertebrate genome could not achieve its complexity without large scale whole-genome duplications. The "two rounds of genome duplication" hypothesis (2R hypothesis) came about, and gained in popularity, especially among developmental biologists.{{Cite book |last=Ohno |first=Susumu |title=Evolution by gene duplication |date=1970 |publisher=Allen & Unwin [u.a.] |isbn=978-0-04-575015-3 |location=London}}

Some researchers have questioned the 2R hypothesis because it predicts that vertebrate genomes should have a 4:1 gene ratio compared with invertebrate genomes, and this is not supported by findings from the 48 vertebrate genome projects available in mid-2011. For example, the human genome consists of ~20,500 protein coding genes according to counts from the Ensembl genome browser{{Cite journal |last1=Clamp |first1=Michele |last2=Fry |first2=Ben |last3=Kamal |first3=Mike |last4=Xie |first4=Xiaohui |last5=Cuff |first5=James |last6=Lin |first6=Michael F. |last7=Kellis |first7=Manolis |last8=Lindblad-Toh |first8=Kerstin |last9=Lander |first9=Eric S. |date=2007-12-04 |title=Distinguishing protein-coding and noncoding genes in the human genome |journal=Proceedings of the National Academy of Sciences |volume=104 |issue=49 |pages=19428–19433 |doi=10.1073/pnas.0709013104 |doi-access=free |pmc=2148306 |pmid=18040051}} while an average invertebrate genome size is about 15,000 genes. The amphioxus genome sequence provided support for the hypothesis of two rounds of whole genome duplication, followed by loss of duplicate copies of most genes.{{cite journal | vauthors = Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutiérrez EL, Dubchak I, Garcia-Fernàndez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin-I T, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS | display-authors = 6 | title = The amphioxus genome and the evolution of the chordate karyotype | journal = Nature | volume = 453 | issue = 7198 | pages = 1064–71 | date = June 2008 | pmid = 18563158 | doi = 10.1038/nature06967 | bibcode = 2008Natur.453.1064P | doi-access = free }} Additional arguments against 2R were based on the lack of the (AB)(CD) tree topology amongst four members of a gene family in vertebrates. However, if the two genome duplications occurred close together, we would not expect to find this topology.{{cite journal | vauthors = Furlong RF, Holland PW | title = Were vertebrates octoploid? | journal = Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume = 357 | issue = 1420 | pages = 531–44 | date = April 2002 | pmid = 12028790 | pmc = 1692965 | doi = 10.1098/rstb.2001.1035 }} A recent study generated the sea lamprey genetic map, which yielded strong support for the hypothesis that a single whole-genome duplication occurred in the basal vertebrate lineage, preceded and followed by several evolutionarily independent segmental duplications that occurred over chordate evolution.{{cite journal | vauthors = Smith JJ, Keinath MC | title = The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications | journal = Genome Research | volume = 25 | issue = 8 | pages = 1081–90 | date = August 2015 | pmid = 26048246 | pmc = 4509993 | doi = 10.1101/gr.184135.114 }}

• Gene duplication
• Genomics
• Karyotype
• Ploidy
• Polyploidy
• Speciation

{{Reflist|32em}}

{{refbegin|32em}}

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