Protein nonadditive expression and solubility in Arabidopsis hybrids and allotetraploids

Abstract

Interspecific hybridization in plants often leads to allopolyploids including most important crops such as wheat, cotton, and canola, while many other crops such as corn and sorghum are grown as hybrid. Both allopolyploids and hybrids show hybrid vigor or heterosis. The phenomenon has been widely applied in agriculture and extensively studied at the genetic and gene expression levels. However, proteomic changes in hybrids and polyploids remain poorly understood. Here, we report comparative analysis of soluble and insoluble proteomes in Arabidopsis intraspecific and interspecific hybrids or allotetraploids formed between A. thaliana and A. arenosa. Both allotetraploids and intraspecific hybrids displayed nonadditive expression (unequal to the sum of the two parents) of the proteins, most of which were involved in biotic and abiotic stress responses. In the allotetraploids, homoeolog-expression bias was not observed among all proteins examined but could occur among 17-20% of the nonadditively expressed proteins, consistent with the transcriptome results. Among expression-biased homoeologs, there were more A. thaliana-biased than A. arenosa-biased homoeologs. Analysis of the insoluble and soluble proteomes revealed more soluble proteins in the hybrids than their parents but not in the allotetraploids. Most proteins in ribosomal biosynthesis and in the thylakoid lumen, membrane, and stroma were in the soluble fractions, indicating a role of protein stability in photosynthetic activities for promoting growth. These results collectively support roles of nonadditive expression of stress-responsive proteins and increased solubility of photosynthetic proteins in Arabidopsis hybrids and allotetraploids, which may promote hybrid vigor. Plain Language SummaryWe analyzed fractionated proteomes to test protein abundance and solubility in Arabidopsis hybrids and polyploids. Many proteins in stress-responses are nonadditively expressed in intraspecific hybrids or allotetraploids. There are more soluble proteins of ribosomal biosynthesis and photosynthetic activities in the hybrids than in their parents but not in allotetraploids. Expression levels are equal among most protein homoeologs in the allotetraploids but are biased for ~20% of nonadditively expressed proteins. Nonadditive protein expression and solubility may play a role in heterosis.