Genome-wide analysis revealed the stepwise origin and functional diversification of HSDs from lower to higher plant species

Noor Saleem; Usman Aziz; Muhammad Ali; Xiangling Liu; Khairiah Mubarak Alwutayd; Rana M Alshegaihi; Gniewko Niedbała; Amr Elkelish; Meng Zhang

doi:10.3389/fpls.2023.1159394

Genome-wide analysis revealed the stepwise origin and functional diversification of HSDs from lower to higher plant species

Front Plant Sci. 2023 Jun 15:14:1159394. doi: 10.3389/fpls.2023.1159394. eCollection 2023.

Authors

Noor Saleem¹, Usman Aziz¹, Muhammad Ali², Xiangling Liu¹, Khairiah Mubarak Alwutayd³, Rana M Alshegaihi⁴, Gniewko Niedbała⁵, Amr Elkelish^{6

7}, Meng Zhang¹

Affiliations

¹ College of Agronomy, Northwest A & F University, Yangling, China.
² College of Horticulture, Northwest A & F University, Yangling, China.
³ Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.
⁴ Department of Biology, College of Science, University of Jeddah, Jeddah, Saudi Arabia.
⁵ Department of Biosystems Engineering, Faculty of Environmental and Mechanical Engineering, Poznań University of Life Sciences, Poznań, Poland.
⁶ Biology Department, College of Science, Imam Mohammad ibn Saud Islamic University (IMSIU), Riyadh, Saudi Arabia.
⁷ Botany Department, Faculty of Science, Suez Canal University, Ismailia, Egypt.

Abstract

Hydroxysteroid dehydrogenase (HSDs) is an oil-body sterol protein (steroleosin) with an NADP(H) binding domain that belongs to the short-chain dehydrogenase/reductase (SDR) superfamily. There are numerous studies on the characterization of HSDs in plants. However, thus far, the evolutionary differentiation and divergence analysis of these genes remain to be explored. The current study used an integrated method to elucidate the sequential evolution of HSDs in 64 sequenced plant genomes. Analyses were conducted on their origins, distribution, duplication, evolutionary paths, domain functions, motif composition, properties, and cis-elements. Results indicate that except for algae, HSD1 was widely distributed in plant species ranging from lower to higher plants, while HSD5 was restricted to terrestrial plants, and HSD2 was identified in fewer monocots and several dicot plants. Phylogenetic analysis of HSD proteins revealed that monocotyledonous HSD1 in moss and ferns appeared closest to the outgroup, V. carteri HSD-like, M. musculus HSD1, and H. sapiens HSD1. These data support the hypothesis that HSD1 originated in bryophytes and then in non-vascular and vascular plants, followed by HSD5 only in land plants. Gene structure analysis suggests that HSDs in plant species came up with a fixed number of six exons, and the intron phase was primarily 0, 1, 0, 0, and 0. Similarly, duplication analysis revealed that segmental duplications were the main reason for HSDs in plant species. Physicochemical properties suggest that dicotyledonous HSD1s and HSD5s were mainly acidic. The monocotyledonous HSD1s and HSD2s and the dicotyledonous HSD2s, HSD3s, HSD4s, and HSD6s were mainly basic, implying that HSDs in plants may have a variety of functions. Cis-regulatory elements and expression analysis revealed that HSDs in plants might have roles in several abiotic stresses. Due to the high expression of HSD1s and HSD5s in seeds, these HSDs in plants may have roles in fatty acid accumulation and degradation.

Keywords: HSDs; NADP(H); SDR; oil body; seed development; steroleosins.

Grants and funding

This work was supported by the National Natural Science Foundation of China (31972964, 32171837), the Key International Cooperation Project of Shaanxi Province (2020KWZ-012), and the Programme of Introduction Talents of Innovative Discipline to Universities (Project 111), (#B18042) 'Crop breedingfor Disease Resistance and Genetic Improvement. Also this paper is funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2023R402), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.