Tissue‐specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus

Abstract

Summary• Recent years have seen rapid advances in our knowledge of the transcriptomic consequences of allopolyploidy, primarily through the study of polyploid crops and model systems. However, few studies have distinguished between homoeologs and between tissues, and still fewer have examined young natural allopolyploid populations of independent origin, whose parental species are still present in the same location.• Here, we examined the expression of 13 homoeolog pairs in seven tissues of 10 plants of allotetraploid Tragopogon mirus from two natural populations formed by independent polyploidizations between Tragopogon dubius and Tragopogon porrifolius c. 40 generations ago. We compare these with patterns of expression in the diploid parental species from the same locality.• Of the 910 assays in T. mirus, 576 (63%) showed expression of both homoeologs, 63 (7%) showed no expression of either homoeolog, 186 (20%) showed nonexpression of one homoeolog across all tissues of a plant, and 72 (8%) showed non-expression of a homoeolog in a particular tissue within a plant. We found two cases of reciprocal tissue-specific expression between homoeologs, potentially indicative of subfunctionalization.• Our study shows that tissue-specific silencing, and even apparent subfunctionalization, can arise rapidly in the early generations of natural allopolyploidy.

The legacy of diploid progenitors in allopolyploid gene expression patterns

“…This leaves 3% of assays that showed novel changes in the control of homoeologue expression subsequent to allopolyploidization. For two of the 13 genes in the T. mirus study [82], peroxisomal NAD-malate dehydrogenase (MD) and peroxidase (PA), tissue-specific silencing was observed in the diploid parental species. It is these cases that would have been of particular interest to Gottlieb as they could give a legacy of tissue-specific homoeologue silencing in allopolyploids that could be spuriously attributed to gene expression changes since allopolyploidization if the parental gene expression patterns were not known.…”

“…( [82], p. 182) Taking all 13 of the genes in this study of T. mirus together, there are 72 cases of tissue-specific gene expression in the allopolyploids, where one homoeologue is expressed and one is not, of which 18% might be due to a legacy of tissue-specific gene silencing from diploid parents (table 1).…”

“…Expression of 13 genes was examined using CAPS, in up to seven tissues, in 10 plants of T. mirus and two plants of each of its diploid parental species, T. porrifolius and T. dubius, randomly sampled from local natural populations [82]. For 11 of these genes, expression was found in all tissues of the parental diploid species.…”

“…Since Gottlieb's experiments on these species, experiments have been done using CAPS analyses on DNA reversetranscribed from RNA; this method assays for single nucleotide differences between homoeologous gene copies at restriction enzyme cut sites [46,82]. Subsequent experiments used Sequenom MassARRAY technology, which can give relative measures of the expression of each homoeologue in an allopolyploid [46].…”

Patterns of chromosomal variation in natural populations of the neoallotetraploid Tragopogon mirus (Asteraceae)

“…To generate a FISH probe for the β-fructosidase gene, we first searched assembled transcriptome sequence data from T. dubius (Buggs et al, 2010) using tBLASTx (Altschul et al, 1997) and querying with a partial β-fructosidase coding sequence (GenBank accession number: DQ267230; Tate et al, 2006). Primers were then designed as close as possible to the beginning and end of a tentative transcript that showed 99% similarity to the query (BFRUCT_1F: 5′-GAGGTTTCCGGTACACATCA-3′ and BFRUCT_2043R: 5′-AACGAC AATCATCATGCCACG-3′).…”