The sources I’ve seen attribute the coinage of ”genome” to botanist Hans Winkler (1920, p. 166).
The pertinent passage goes:
Ich schlage vor, für den haploiden Chromosomensatz, der im Verein mit dem zugehörigen Protoplasma die materielle Grundlage der systematischen Einheit darstellt den Ausdruck: das Genom zu verwenden … I suggest to use the expression ”the genome” for the haploid set of chromosomes, which together with the protoplasm it belongs with make up the material basis of the systematic unit …
That’s good, but why did Winkler need this term in the first place? In this chapter, he is dealing with the relationship between chromosome number and mode of reproduction. Of course, he’s going to talk about hybridization and ploidy, and he needs some terms to bring order to the mess. He goes on to coin a couple of other concepts that I had never heard of:
… und Kerne, Zellen und Organismen, in denen ein gleichartiges Genom mehr als einmal in jedem Kern vorhanden ist, homogenomatisch zu nennen, solche dagegen, die verschiedenartige Genome im Kern führen, heterogenomatisch.
So, a homogenomic organism has more than one copy of the same genome in its nuclei, while a heterogenomic organism has multiple genomes. He also suggests you could count the genomes, di-, tri- up to polygenomic organisms. He says that this is a different thing than polyploidy, which is when an organism has multiples of a haploid chromosome set. Winkler’s example: A hybrid between a diploid species with 10 chromosomes and another diploid species with 16 chromosomes might have 13 chromosomes and be polygenomic but not polyploid.
These terms don’t seem to have stuck as much, but I found them used here en there, for example in papers on bananas (Arvanitoyannis et al. 2008) and cotton (Brown & Menzel 1952); cooking bananas are heterogenomic.
This only really makes sense in cases with recent hybridisation, where you can trace different chromosomes to origins in different species. You need to be able to trace parts of the hybrid genome of the banana to genomes of other species. Otherwise, the genome of the banana just the genome of the banana.
Analogously, we also find polygenomes in this cancer paper (Navin et al. 2010):
We applied our methods to 20 primary ductal breast carcinomas, which enable us to classify them according to whether they appear as either monogenomic (nine tumors) or polygenomic (11 tumors). We define ”monogenomic” tumors to be those consisting of an apparently homogeneous population of tumor cells with highly similar genome profiles throughout the tumor mass. We define ”polygenomic” tumors as those containing multiple tumor subpopulations that can be distinguished and grouped by similar genome structure.
This makes sense; if a tumour has clones of cells in it with a sufficiently rearranged genome, maybe it is fair to describe it as a tumour with different genomes. It raises the question what is ”sufficiently” different for something to be a different genome.
How much difference can there be between sequences that are supposed to count as the same genome? In everything above, we have taken a kind of typological view: there is a genome of an individual, or a clone of cells, that can be thought of as one entity, despite the fact that every copy of it, in every different cell, is likely to have subtle differences. Philosopher John Dupré (2010), in ”The Polygenomic Organism”, questions what we mean by ”the genome” of an organism. How can we talk about an organism having one genome or another, when in fact, every cell in the body goes through mutation (actually, Dupré spends surprisingly little time on somatic mutation but more on epigenetics, but makes a similar point), sometimes chimerism, sometimes programmed genome rearrangements?
The genome is related to types of organism by attempts to find within it the essence of a species or other biological kind. This is a natural, if perhaps naïve, interpretation of the idea of the species ‘barcode’, the use of particular bits of DNA sequence to define or identify species membership. But in this paper I am interested rather in the relation sometimes thought to hold between genomes of a certain type and an individual organism. This need not be an explicitly essentialist thesis, merely the simple factual belief that the cells that make up an organism all, as a matter of fact, have in common the inclusion of a genome, and the genomes in these cells are, barring the odd collision with a cosmic ray or other unusual accident, identical.
Dupré’s answer is that there probably isn’t a universally correct way to divide living things into individuals, and what concept of individuality one should use really depends on what one wants to do with it. I take this to mean that it is perfectly fine to gloss over real biological detail, but that we need to keep in mind that they might unexpectedly start to matter. For example, when tracing X chromosomes through pedigrees, it might be fine to ignore that X-inactivation makes female mammals functionally mosaic–until you start looking at the expression of X-linked traits.
Finally, the genome exists not just in the organism, but also in the computer, as sequences, maps and obscure bioinformatics file formats. Arguably, keeping the discussion above in mind, the genome only exists in the computer, as a scientific model of a much messier biology. Szymanski, Vermeulen & Wong (2019) investigate what the genome is by looking at how researchers talk about it. ”The genome” turns out to be many things to researchers. Here they are writing about what happened when the yeast genetics community created a reference genome.
If the digital genome is not assumed to solely a representation of a physical genome, we might instead see ”the genome” as a discursive entity moving from the cell to the database but without ever removing ”the genome” from the cell, aggregating rather than excluding. This move and its inherent multiplying has consequences for the shape of the community that continues to participate in constructing the genome as a digital text. It also has consequences for the work the genome can perform. As Chadarevian (2004) observes for the C. elegans genome sequence, moving the genome from cell to database enables it to become a new kind of mapping tool …
Consequently, the informational genome can be used to manufacture coherence across knowledge generated by disparate labs by making it possible to line up textual results – often quite literally, in the case of genome sequences as alphabetic texts — and read across them.
Prior to the availability of the reference genome, such coherence across the yeast community was generated by strain sharing practices and standard protocols and notation for documenting variation from the reference strain, S288C, authoritatively embodied in living cells housed at Mortimer’s stock center. After the sequencing project, part of that work was transferred to the informational, textual yeast genome, making the practice of lining up and making the same available to those who worked with the digital text as well as those who worked with the physical cell.
And that brings us back to Winkler: What does the genome have in common? That it makes up the basis for the systematic unit, that it belongs to organisms that we recognize as closely related enough to form a systematic unit.
Winkler H. (1920) Verbreitung und Ursache der Parthenogenesis im Pflanzen- und Tierreiche.
Arvanitoyannis, Ioannis S., et al. ”Banana: cultivars, biotechnological approaches and genetic transformation.” International journal of food science & technology 43.10 (2008): 1871-1879.
Navin, Nicholas, et al. ”Inferring tumor progression from genomic heterogeneity.” Genome research 20.1 (2010): 68-80.
Brown, Meta S., and Margaret Y. Menzel. ”Polygenomic hybrids in Gossypium. I. Cytology of hexaploids, pentaploids and hexaploid combinations.” Genetics 37.3 (1952): 242.
Dupré, John. ”The polygenomic organism.” The Sociological Review 58.1_suppl (2010): 19-31.
Szymanski, Erika, Niki Vermeulen, and Mark Wong. ”Yeast: one cell, one reference sequence, many genomes?.” New Genetics and Society 38.4 (2019): 430-450.