Abstract
BackgroundGenome doubling may have multi-level effects on the morphology, viability and physiology of polyploids compared to diploids. We studied the changes associated with autopolyploidization in two systems of somatic newly induced polyploids, diploid-autotetraploid and triploid-autohexaploid, belonging to the genus Hylocereus (Cactaceae). Stomata, fruits, seeds, embryos, and pollen were studied. Fruit pulp and seeds were subjected to metabolite profiling using established gas chromatography-mass spectrometry (GC-MS) and ultra-performance liquid chromatography (UPLC) Q-TOF-MS/MS (time of flight)-protocols.ResultsAutopolyploid lines produced lower numbers of tetrads, larger pollen grains with lower viability, larger stomata with lower density, and smaller fruits with lower seed numbers and decreased seed viability. The abundance of sugars was lower in the fruits and seeds of the two duplicated lines than in their donor lines, accompanied by increased contents of amino acids, tricarboxylic acid (TCA) cycle intermediates, organic acids and flavonoids. Betacyanins, the major fruit pigments in diploid and triploid donors, decreased following genome doubling. Both autopolyploid Hylocereus lines thus exhibited unfavorable changes, with the outcome being more dramatic in the autohexaploid than in the autotetraploid line.ConclusionInduced autotetraploid and autohexaploid lines exhibited morphological and cytological characteristics that differed from those of their donor plants and that were accompanied by significant metabolic alterations. It is suggested that a developmental arrest occurs in the fruits of the autohexaploid line, since their pericarp shows a greater abundance of acids and of reduced sugars. We conclude that genome doubling does not necessarily confer a fitness advantage and that the extent of alterations induced by autopolyploidization depends on the genetic background of the donor genotype.
Highlights
Genome doubling may have multi-level effects on the morphology, viability and physiology of polyploids compared to diploids
An increase in fluorescence intensity, showing a doubling or close to doubling, in total 2C-DNA was observed in both autopolyploid lines vis-à-vis their respective control lines (Table 1 and Additional file 1), i.e., 4.2 ± 0.1 pg/ 2C for the diploid H. monacanthus vs. 8.0 ± 0.4 pg/2C for the autotetraploid line D-27, and 5.9 ± 0.3 pg/2C for the allotriploid S-75 vs. 13.7 ± 0.1 pg/2C, for the autohexaploid line D-2.3 (Table 1)
Principal component analysis (PCA) performed for both fruit pulp and seed samples using these 12 most abundant metabolites showed that the autotetraploid and the diploid donor H. monacanthus exhibited comparable metabolic profiles, but there were clear differences between the autohexaploid and the donor allotriploid S-75; these findings implied that the effect of autopolyploidization on secondary metabolism was more significant for the fruits produced by the autohexaploid line (Figure 3C)
Summary
Genome doubling may have multi-level effects on the morphology, viability and physiology of polyploids compared to diploids. Metabolic alterations that arise from chromosome duplication have been investigated only in a limited number of studies, and those studies have targeted only specific secondary metabolites, e.g., flavonols and alkaloids, and have “missed” the global metabolic changes associated with autopolyploidization. In several species, such as Chamomilla recutita, Petunia Mitchell, Salvia miltiorrhiza, Artemisia annua, and Panax ginseng, the production of flavonoids and terpenoids per gram of tissue was higher in polyploids than in their diploid counterparts [29,30,31,32,33]
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