Lessons from Natural and Artificial Polyploids in Higher Plants

Abstract

Polyploidy in higher plants is a major source of genetic novelty upon which selection may act to drive evolution, as evidenced by the widespread success of polyploid species in the wild. However, research into the effects of polyploidy can be confounded by the entanglement of several processes: genome duplication, hybridisation (allopolyploidy is frequent in plants) and subsequent evolution. The discovery of the chemical agent colchicine, which can be used to produce artificial polyploids on demand, has enabled scientists to unravel these threads and understand the complex genomic changes involved in each. We present here an overview of lessons learnt from studies of natural and artificial polyploids, and from comparisons between the 2, covering basic cellular and metabolic consequences through to alterations in epigenetic gene regulation, together with 2 in-depth case studies in Senecio and Glycine. See also the sister article focusing on animals by Arai and Fujimoto in this themed issue.

Evolution of physiological responses to salt stress in hexaploid wheat

“…transcriptional rewiring | Na + homeostasis | salinity tolerance P olyploidy or whole genome duplication (WGD) is a pervasive, driving force in plant and vertebrate evolution, which has fascinated biologists for more than a century (1,2). The common occurrence of WGD suggests an evolutionary advantage of having multiple genomes at least in certain circumstances, which might have enabled the polyploid organisms to be better adapted to some adverse environmental conditions than their diploid progenitors (3,4).…”

The shock of being united and symphiliosis

“…18,[34][35][36]39 However substantial the genomic restructuring is, "by far, the most striking change to regulation of gene expression in allopolyploids… is that of epigenetic modification". 40 Some of these modifications are also similar to those found in cancers and include genome-wide alterations in cytosine methylation, gene silencing or activation, alteration of gene imprinting, gene non-functionalization, subfunctionalization, neo-functionalization, changes in mRNA splicing and in gene expression. 30,35,41 Of particular interest are emergent, or so-called non-additive patterns of gene expression, as they can result in new, potentially advantageous phenotypes.…”

“…2). Several aspects of this process have been named the genomic 36 or transcriptome 40 shock, a conflict zone, 43 parental squabbles, 48 nuclear reprogramming, 60 and the problem of colliding networks. 44 To acknowledge the existence of this process and to have a term to refer to it as a whole, I suggest calling it symphiliosis, from a Greek word for reconciliation, "συμϕιλίωση", and, accordingly, referring to all interrelated instabilities associated with symphiliosis, of which we probably know only some, as symphilial instability, or SIN.…”

“…this act of creation corresponds to the transcriptome shock. 40 Being on a slope, the network "slides" into an attractor corresponding to a cell type distinct from either of the parental types, hence the emergent properties of the hybrids. this transition is manifested by changes in gene expression that appear chaotic and the instability that continues until the attractor is reached.…”

“…30,35,41 Of particular interest are emergent, or so-called non-additive patterns of gene expression, as they can result in new, potentially advantageous phenotypes. 29,[40][41][42] To begin explaining how allopolyploidy causes genomic and epigenetic changes, Barbara McClintock suggested that uniting two distinct genomes in one nucleus is a type of stress, which she named "genomic shock", that triggers restructuring and integration of the parental genomes, 36 but what this stress is, how it is sensed, and how this information is translated into genome restructuring is still unknown. 40,43 By analogy with the genomic shock, the cause of the gene expression changes has been termed the transcriptome shock, 40 to indicate that uniting two different expression patterns is also a type of stress.…”