Academic journal article Genetics

Hybrid Decay: A Transgenerational Epigenetic Decline in Vigor and Viability Triggered in Backcross Populations of Teosinte with Maize

Academic journal article Genetics

Hybrid Decay: A Transgenerational Epigenetic Decline in Vigor and Viability Triggered in Backcross Populations of Teosinte with Maize

Article excerpt

PLANT breeders seek to develop improved varieties through crosses among different individuals of a species followed by selection. New combinations of alleles can lead to improved performance, allowing development of elite varieties. In many plant species, the direct combination of genetic information in the two parents can lead to hybrid vigor (heterosis). In other cases, there can be deleterious consequences of crossing individuals that is often referred to as hybrid incompatibility. This phenomenon has been particularly wellstudied for crosses between members of related species (Bomblies and Weigel 2007; Rieseberg and Blackman 2010; Fishman and Sweigart 2018). Even within a species there are examples of combinations that can lead to reduced vigor or fertility (Bomblies 2010). In some classic examples, hybrid incompatibility is caused by chromosomal rearrangements such as inversions or translocations that can result in partial sterility (Fishman and Sweigart 2018).

Maize geneticists have a long history of crossing maize (Zea mays ssp. mays) and its wild relatives, the annual Mexican teosintes (Z. mays ssp. parviglumis or Z. mays ssp. mexicana) for a variety of reasons. Beadle studied chromosome pairing in maize-teosinte hybrids and the inheritance of domestication traits in a maize-teosinte F2 population (Beadle 1932, 1972). Kermicle studied pollen-pistil incompatibility in maize-teosinte hybrids and their derivatives (Kermicle 2006). Multiple QTL studies have mapped the genes controlling domestication traits in maize-teosinte hybrid populations (e.g., Doebley and Stec 1991; Briggs et al. 2007). Other studies have utilized populations derived from maize X teosinte crosses to map and identify key domestication genes including teosinte branched 1 (tbl), teosinte glume architecture (tga1), and prolificacy 1.1 (prol1.1) (Doebley et al. 1997; Wang et al. 2005; Wills et al. 2013). Finally, two projects assayed the effects of teosinte chromosome segments introgressed into maize on a variety of domestication and agronomic traits (Studer and Doebley 2012; Liu et al. 2016). Although there are a few known chromosomal inversions that are polymorphic in teosinte and maize (Fang et al. 2012) and a few polymorphic factors for pollen-pistil compatibility that can prevent hybrid formation (Lu et al. 2014), there are no reports of a severe loss of vigor or viability among maize-teosinte hybrids or their descendant lines.

During the construction mapping populations to study the effects of teosinte alleles, we noted an unusual sickly syndrome in the backcross progeny resulting from crosses of maize with teosinte from near the Valle de Bravo in the state of Mexico, hereafter "Bravo" teosinte. The initial F1 hybrids are normal, but a sickly phenotype is observed in the Backcross 1 (BC1) and is more pronounced in subsequent backcross generations. Once the sickly phenotype appears in a lineage, healthy plants are never recovered by additional backcrosses to the normal maize parent. The inheritance pattern for the hybrid decay syndrome does not depend upon inheritance of specific chromosomal segments from the teosinte parent and does not segregate in backcross populations. We documented genomic instability in these backcross populations with increased copy number for specific sequences some with homology to transposable elements (TEs). De novo assembly of transcripts identifies a collection of upregulated sequences including some that have little or no similarity to sequences in the genomes of the maize recurrent parents (W22 or B73). Although the global patterns of DNA methylation and small RNA (sRNA) production are similar between sickly and normal plants, some TEs and sequences that are upregulated in sickly plants show altered methylation and sRNA profiles. Our observations suggest that crosses between Bravo teosinte and maize can trigger genomic instability that is inherited in all progeny. We name this phenomenon "hybrid decay," a transgenerational decline in vigor and viability triggered in backcross populations of Bravo teosinte with maize. …

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