Identification, Characterization and Function of Orphan Genes Among the Current Cucurbitaceae Genomes

Abstract

Orphan genes (OGs) that are missing identifiable homologs in other lineages may potentially make contributions to a variety of biological functions. The Cucurbitaceae family consists of a wide range of fruit crops of worldwide or local economic significance. To date, very few functional mechanisms of OGs in Cucurbitaceae are known. In this study, we systematically identified the OGs of eight Cucurbitaceae species using a comparative genomics approach. The content of OGs varied widely among the eight Cucurbitaceae species, ranging from 1.63% in chayote to 16.55% in wax gourd. Genetic structure analysis showed that OGs have significantly shorter protein lengths and fewer exons in Cucurbitaceae. The subcellular localizations of OGs were basically the same, with only subtle differences. Except for aggregation in some chromosomal regions, the distribution density of OGs was higher near the telomeres and relatively evenly distributed on the chromosomes. Gene expression analysis revealed that OGs had less abundantly and highly tissue-specific expression. Interestingly, the largest proportion of these OGs was significantly more tissue-specific expressed in the flower than in other tissues, and more detectable expression was found in the male flower. Functional prediction of OGs showed that (1) 18 OGs associated with male sterility in watermelon; (2) 182 OGs associated with flower development in cucumber; (3) 51 OGs associated with environmental adaptation in watermelon; (4) 520 OGs may help with the large fruit size in wax gourd. Our results provide the molecular basis and research direction for some important mechanisms in Cucurbitaceae species and domesticated crops.

Research Advances and Prospects of Orphan Genes in Plants

“…Ms2 gene also plays a pivotal role in wheat breeding, providing higher yields of hybrid wheat. Similarly, 18 OGs were proven to be related to male sterility in watermelon (Citrullus lanatus), and the research also confirmed that 182 OGs were involved in flower development in cucumber (Cucumis sativus), 520 OGs may help with the large fruit size in wax gourd (Benincasa hispida) (Ma et al, 2022). Study showed that 18 CSGs were mainly associated with phenylalanine biosynthesis, biosynthesis of amino acids, pentose phosphate pathway, photosynthesis, and carbon metabolism (Zhao and Ma, 2021).…”

“…The present study has revealed that the OGs play a specific role in primary substance metabolism, species-specific traits' formation, and response to diverse stresses, making them important for lineage-specific adaptations (Figure 1). OGs have a shorter origination time and distinctive features relative to ECGs among all species (Ma et al, 2022). Gene structure analysis showed that OGs exhibit significantly shorter protein length, which mainly attributed to the fewer number of exons, and younger genes have fewer exons.…”

“…The rapid accumulation of genomic data on a large variety of plants will allow increasing integrity of identification of OGs. So far the presence of OGs has been reported in many plants or lineages [such as B. rapa (Jiang et al, 2018), A. thaliana (Yang et al, 2009;Lin et al, 2010;Donoghue et al, 2011;Cui et al, 2015), O. sativa (Guo et al, 2007;Yang et al, 2009;Cui et al, 2015;Jin et al, 2019), P. trichocarpa (Yang et al, 2009), V. unguiculata (Li G. et al, 2019), Poaceae (Campbell et al, 2007), Aegiceras corniculatum (Ma et al, 2021), C. sinensis (Xu et al, 2015), Amaranthus hypochondriacus (Cabrales-Orona and Délano-Frier, 2021), Camellia sinensis (Zhao and Ma, 2021), and eight Cucurbitaceae family members (Ma et al, 2022)]. Every sequenced genome contains OGs whose origins are obscure because of the absence of homologs (Blanco-Melo et al, 2016).…”

“…Furthermore, by mediating crosstalk between primary metabolism and environmental alterations, the QQS gene has also been involved in the optimization and tolerance to biotic/abiotic perturbations (Arendsee et al, 2014;Qi et al, 2019;Tanvir et al, 2022). Recently, 51 OGs were proven to be associated with environmental adaptation in watermelon (Ma et al, 2022).…”

“…Although OGs in different plants have no sequence similarities, they share similar genic features, implying their evolutionary mechanisms could be similar (Ma et al, 2020). The evolutionary origin of OGs is a microevolutionary process, and the study of how OGs arise and differentiate is essential to explain the generation and succession of novel phenotypes and eventually biodiversity (Ma et al, 2022). The relevance between the adaptive evolution and generation of new agronomic traits still needed to be determined.…”