Genomic, Transcriptomic, and Phenomic Variation Reveals the Complex Adaptation of Modern Maize Breeding

Abstract

The temperate-tropical division of early maize germplasms to different agricultural environments was arguably the greatest adaptation process associated with the success and near ubiquitous importance of global maize production. Deciphering this history is challenging, but new insight has been gained from examining 558 529 single nucleotide polymorphisms, expression data of 28 769 genes, and 662 traits collected from 368 diverse temperate and tropical maize inbred lines in this study. This is a new attempt to systematically exploit the mechanisms of the adaptation process in maize. Our results indicate that divergence between tropical and temperate lines apparently occurred 3400-6700 years ago. Seven hundred and one genomic selection signals and transcriptomic variants including 2700 differentially expressed individual genes and 389 rewired co-expression network genes were identified. These candidate signals were found to be functionally related to stress responses, and most were associated with directionally selected traits, which may have been an advantage under widely varying environmental conditions faced by maize as it was migrated away from its domestication center. Our study also clearly indicates that such stress adaptation could involve evolution of protein-coding sequences as well as transcriptome-level regulatory changes. The latter process may be a more flexible and dynamic way for maize to adapt to environmental changes along its short evolutionary history.

A Gene-Oriented Haplotype Comparison Reveals Recently Selected Genomic Regions in Temperate and Tropical Maize Germplasm

“…Previous research suggests that improvement and adaptation in maize may not have been a sequential and discrete process, but was rather an overlapping process [13]. Thus, we focused on the selected genes involved in flowering, one of most important gene sets for adaptation, by examining two hundred flowering candidate genes from a previous study [20].…”

“…Using this method, evidence for selection across the genome during maize domestication and improvement was evaluated in teosinte versus maize landraces, and landraces versus improved lines, respectively [4]. This same method was also used to reveal complex adaptation in maize worldwide by comparing tropical and temperate lines [13]. The XP-CLR approach is designed to detect “ancient” signature bottlenecks from several thousand years ago, while the cross population extended haplotype heterozygosity (XP-EHH) test, a haplotype-base approach, is designed to detect recently fixed or high frequency alleles in selective sweeps through population comparisons [14].…”

“…As an alternative to genomic resequencing, RNA sequencing technology, which defines both sequence and expression divergence [16], provides a cost effective way to explore even larger groups of inbred lines [13]. In addition, information about differential expression also provides an opportunity to examine the global consequences of gene expression in relation to selection pressure [17].…”

Exploring Identity-By-Descent Segments and Putative Functions Using Different Foundation Parents in Maize

“…To evaluate the genomic and phenotypic characteristics of maize germplasm and help breeders develop new inbred lines and predict hybrid performance, many studies have focused on maize genetic differentiation [12, 13], pedigree information [14], and the genetic bases of complex traits using different panels with multiple sources, different molecular markers and differentiation patterns of maize germplasm from different ecological environments [15, 16]. For U.S. maize breeding, three main heterotic groups, i.e., Iowa Stiff Synthetic (SS), Non-Stiff Stalk (NSS) and Iodent (IDT), were formed in the late 1950s and constitute genetically distinct breeding pools today [3], with representative lines of B73, Mo17 and 207, respectively.…”

“…Using the same strategy, Jiao and his colleagues analyzed the genomic differentiation among 278 temperate lines and identified extensive variable regions [28], but the relevant functions of these regions remain unknown. By combining genomic, transcriptomic and phenotypic analysis, the divergence between tropical and temperate lines and many genes involved in stress adaption were identified by Liu et al [13], and the complex genetic networks during the improvement of maize adaptation were revealed. Most previous studies have addressed the relationships among maize accessions with different origins and clarified some important genetic networks of complex traits.…”