Genome-wide identification and characterization of the CKII gene family in the cultivated banana cultivar (Musa spp. cv Tianbaojiao) and the wild banana (Musa itinerans)

RESEARCH ARTICLE Genome-wide identification and characterization of the CKII gene family in the cultivated banana cultivar (Musa spp. cv Tianbaojiao) and the wild banana (Musa itinerans) Weihua Liu, Zhengchun Lin, Yanying Liu, Yuling Lin, XuHan Xu, Zhongxiong Lai* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Liu W, Lin Z, Liu Y, Lin Y, Xu X, Lai Z (2018) Genome-wide identification and characterization of the CKII gene family in the cultivated banana cultivar (Musa spp. cv Tianbaojiao) and the wild banana (Musa itinerans). PLoS ONE 13(7): e0200149. https://doi.org/ 10.1371/journal.pone.0200149 Editor: Hong Zhang, Texas Tech University, UNITED STATES Received: January 22, 2018 Accepted: June 20, 2018 Published: July 11, 2018 Copyright: © 2018 Liu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by the earmarked Fund for China Agriculture Research System (CARS-31-15) and the Science and Technology Major Science and Technology Project in Fujian Province of China (2015NZ20002-1) (ZL). The funders had no role in study design, data Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China * Abstract Plant casein kinase II (CKII) plays an essential role in regulating plant growth and development, and responses to biotic and abiotic stresses. Here, we report the identification and characterization of the CKII family genes in Musa spp. cv. ‘Tianbaojiao’ (AAA group) and the wild banana (Musa itinerans). The 13 cDNA sequences of the CKII family members were identified both in ‘Tianbaojiao’ and wild banana, respectively. The differences between CKII α and CKII β members are corroborated through the subcellular localizations, phosphorylation sites and gene structures. The cloning of CKII β-like-2 gDNA sequences in wild banana and ‘Tianbaojiao’ and the analysis of gene structures showed MiCKIIβ-like-2b and MaCKIIβ-like-2 are likely alternatively spliced transcripts, which were derived from the alternative splicing events that involved exon deletion. The qPCR validation showed differential expression CKII family members in response to cold stress and also in all tested tissues (leaf, pseudostem and root) of wild banana. In particular, the normal transcript MiCKIIβ-like2a was highly expressed in response to cold stress in wild banana; oppositely, the alternatively spliced transcript MiCKIIβ-like-2b was quite lowly expressed. The complex origin and long-term evolution of Musa lineage might explain the alternative splicing events of CKII βlike-2. Introduction Casein kinase II (CKII or CK2) is a Ser/Thr kinase involved in the regulation of protein functions in eukaryotes. Plant CKII is a tetrameric protein composed of two catalytic (α) and two regulatory (β) subunits, and it is also a pleiotropic enzyme. It plays an essential role in regulating various cellular processes such as growth, development, circadian rhythms, light responses, hormone responses, transcription, translation, cell-cycle regulation, nuclear transport, Ca2+ storage, seed storage, salicylic acid-mediated defenses, flowering time, DNA repair and responses to biotic and abiotic stresses in plants, such as maize, tobacco, wheat, mustard and PLOS ONE | https://doi.org/10.1371/journal.pone.0200149 July 11, 2018 1 / 18 Genome-wide identification and characterization of CKII gene family in the cultivated and the wild bananas collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Arabidopsis thaliana [1–13]. Salinas et al (2006) [14] presented a complete survey of the CKII gene family and found four α subunits and four β subunit genes, which were all expressed in the inflorescences, stems, leaves and roots in Arabidopsis. Mulekar et al (2012) [4] further reported that CKII α subunits affect multiple developmental and stress-responsive pathways in Arabidopsis. Portoles and Mas (2010) [15] found that the functional interplay between CKII and CCA1 (circadian clock associated 1) transcriptional activities is essential for clock temperature compensation in Arabidopsis. In plant cells, CKII is localized in the cytosol and the nucleus [16], and α subunits of the CKII family members are localized in the chloroplasts in mustard and Arabidopsis [8]. CKII is an extremely conserved pleiotropic protein kinase with more than 300 substrates [6,17]. The CKII phosphor acceptor sites are specified by multiple acidic residues, with the one at position +3 relative to the target residue being crucial. The CKII holoenzyme is composed of two catalytic subunits (αα, α’α’ or αα’), which act mainly as catalysts of phosphorylation, and a dimer of two non-catalytic β subunits, which act mainly as regulators of enzymatic activities [2,4,17]. Dennis and Browning (2009) reported the differential phosphorylation of plant translation initiation factors by Arabidopsis thaliana CKII holoenzymes [18]. Recent plant whole-genome sequencing projects will allow the precise structure and function of CKII to be full characterized. Banana belongs to the genus Musa, a member of the family Musaceae, and is the most popular fruit in the worldwide. It is thermophilic crop, and distribute in the warm tropical or subtropical regions. Fujian province, in the northern margin of China is one such region prominent for banana cultivation. ‘Tianbaojiao’, which is the famous traditional cultivar in Fujian, often suffered low temperature stress in winter and early spring (S1 Fig). The critical temperature of growth is thought to be around 13˚C for most banana cultivars in China [19]. The morphological changes of ‘Tianbaojiao’ leaves were quite different at low temperature stress (4˚C) and when the treatment time was increased. The changes such as slight water logging (3 h), wilting (5–7 h) or death (at 28˚C to recover) were observed (S2 Fig). The wild banana genetic resources are abundant in China, particularly in Fujian province. A novel wild banana line, which was found at Sanming city, Fujian province, is thought to be extremely cold resistant based on screening the wild banana genetic resources collected by our team for over 10 years [20]. It can grow well around 0˚C [21], and its semilethal temperature was lower than other nine Musa genus plants, reached as low as -1.776˚C [22]. So the wild banana (coldresistant) and ‘Tianbaojiao’ (cold-sensitive) were used as materials to study the existence and expression of CKII family genes. The banana genome has been published [23–24], allowing for the identification of CKII family genes in banana. In this stu (...truncated)