The plasticity of plant genomes: Causes and consequences: a survey of data on structural genome variation in plants

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During recent years knowledge on genome plasticity has vastly increased. For this reason, COGEM has expressed the need for an up-to-date inventory of spontaneous genome changes in eukaryotes with an emphasis on plants, and in particular, the structural changes that occur during conventional breeding and
cultivation of crops. This information is relevant for risk assessment of “intragenic” crops, where new combinations of genetic elements from the host (or crossable) species may be introduced. The central question is whether such new combinations also can arise spontaneously in conventional breeding,
including conventional mutagenesis, and at what frequency. This contributes to establishing a “baseline” against which “intragenesis,” or the creation of new structural variation in general, will be compared in risk assessment. The report focusses on “Structural Variation” (SV) in genomes: differences between genomes
of individuals of the same (or crossable) species, larger than 50 base pairs. This includes deletions, insertions (including transposable elements), duplications, inversions, translocations, and complex rearrangements.
For this report, we used two sources of information: a literature search, and interviews with professionals in plant breeding companies about their experience with SV in their work. The latter led to the conclusion that SV probably plays a (yet mostly unknown) role in their breeding work, and the examples they were
willing to share were mainly already described in the literature. This report first describes the methods of detection of SVs. Genome-wide detection of SV depends on three techniques: cytology (microscopy), whole-genome (re-) sequencing and its analysis, and hybridisation-based techniques. Unfortunately, these methods still suffer from high false-positive and false-negative rates and low resolution, meaning that even if SV is discovered, its exact nature and effect on genes is usually still mostly unknown. This would require precise sequencing of the SV ‘breakpoint’ or border. Fortunately, the arising long-read sequencing
technologies are already starting to remove these limitations and will do more so soon. Further, a detailed analysis of specific phenotypic traits has provided already more precise insight into the structural variation causing these traits.
The processes themselves that lead to observed SV usually are not witnessed. However, many models have been proposed, which may explain observed SV in retrospect. We describe a series of such models.
The suggested mechanisms leading to SV can be broadly categorised as:
1. “Copying errors” during DNA replication of multiplying cells.
2. Double-strand DNA breaks, followed by repair. This can lead to deletions, inversions, and in the inclusion of “filler” DNA into the repaired breaks.
3. Recombination-based. During meiosis, recombination frequently occurs between allelic sequences of pairing chromosomes. This can lead to duplication, deletion, and translocation.
4. The activity of transposable elements. Transposable Elements or transposons are DNA sequences that can move through genomes by replication and insertion (“copy and paste”) or by excision and reintegration (“cut and paste”).

This study aimed at contributing to a foundation for a sound biosafety assessment of intragenic crops. Therefore, we have focussed on documented SVs between crossable plants. These comparisons reported here should be distinguished from comparisons between related species and genera, which describe changes on a more evolutionary timescale. Several examples of intraspecies SVs, leading to discernible phenotypes or important traits, are described.
Concerning SV that arises during conventional breeding, we also discuss variation caused by “conventional mutagenesis” such as by chemicals or radiation. From the limited available literature, it was concluded that in particular, fast-neutron or heavy-ion irradiation causes SV, mostly large deletions, inversions, and
translocations. Combined with the capacity of double-strand break repair to incorporate filler DNA, and the propensity for translocation, this increases the frequency of creating new combinations of genomic DNA considerably. Further, we review possible effects of tissue culture on SV, but compared to conventional
mutagenesis, little is known about tissue culture’s impact on the creation of new SV.

The amount of available literature decreases sharply when it comes to reports of spontaneous structural changes over one or a few generations, both in plants as well as in other eukaryotes, including humans.
This is partly due to constraints of current sequence technologies and bioinformatics, i.e. the ability to reliably identify and characterise SVs, as well as to their low frequency. Detection methods may improve soon. Mutation accumulation lines, specifically from fast cycling plants with small genomes such as Arabidopsis, are particularly suitable for collecting data on low-frequency events. One example of Arabidopsis siblings over 5 generations is discussed. In that study, resequencing of descendants from mutation accumulation lines specifically identified large deletions and some shorter insertions. The creation
of unique combinations of genome elements was assessed in none of these experiments.
Although the amount of information on spontaneously arising SV during cultivation or plant breeding was limited, we provide several striking examples of structural changes in apple, grape, and tomato, that led to pronounced and often commercially attractive phenotypic traits.
We sorted different types of SV in likely order of decreasing frequencies, i.e.
1. Exchange of genetic elements within a cluster of tandem repeats, such as resulting from unequal crossovers and other nonallelic homologous recombinations;
2. Deletions, including the insertion of filler DNA during repair;
3. Translocations of transposable elements (TEs), including hitch-hiking host DNA;
4. Inverted repeats, leading to RNAi-like structures;
5. Translocations of non-TEs;
6. Inversions;
7. Complex rearrangements
in intragenic example plants. This list is not exhaustive, and the exact order can be disputed. In the case of conventional breeding without mutagenesis, we regard the frequencies of types 1 to 3 sufficiently high for occurring during traditional breeding by crossing and cultivation of crops. When including conventional mutagenesis, types 4 to 6 can also be regarded as occurring rather frequently during conventional breeding.
We provided two examples of intragenic crops. The likelihood of spontaneous creation of such events within one or a few breeding generations is very low
Original languageEnglish
Place of PublicationBilthovem
Number of pages78
Publication statusPublished - 31 Jul 2020

Publication series

NameOnderzoeksrapport / COGEM
No.CGM 2020-04


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