In the process of plant growth and morphogenesis formation, it will respond to the changes in the wavelength, intensity and direction of external light signals, one of which is phototropism in plants, that is, the phenomenon that plant organs bend toward or away from a specific direction of light source (Holland et al., 2009). Arabidopsis phototropin PHOT1 (PHOTOTROPIN1) and PHOT2 (PHOTOTROPIN2) are involved in the regulation of phototropism, chloroplast movement, stomatal opening, leaf extension and localization (Christie et al., 2015). NPH3 (NONPHOTOTROPIC HYPOCOTYL3) and RPT2 (ROOT PHOTOTROPISM2) in Arabidopsis thaliana were identified in molecular genetic analysis of phototropic defect mutants. Studies have shown that NPH3 and RPT2 are involved in phototropism, leaf extension and location regulation mediated by phototropism, while RPT2 also plays a role in chloroplast movement (Christie et al., 2015, Suetsugu et al., 2016, Christie et al., 2018). NPH3 and RPT2 belong to a plant-specific NRL (NPH3/RPH2-Like) family, which mainly consists of three characteristic domains: the BTB (Broad complex, tramtrack, and bric à brac) domain at the N-terminal, the coiled helix domain at the C-terminal and the NPH3 domain in the middle (Motchoulski and Liscum, 1999, Sakai et al., 2000, Liscum et al., 2014). The NPH3 domain is common to the members of the NRL gene family, while some members of the NRL gene family lack the N-terminal BTB domain or the C-terminal coiled helix domain (Pedmale et al., 2010). In the functional studies of the three characteristic domains of NRL gene family, the BTB domain at the N-terminal was involved in the ubiquitination of phot1 mediated by E3 ubiquitin ligase CRL3^NPH3, and the crimp structure at the C-terminal was involved in the protein interaction between NPH3 and phot1. However, the function of NPH3 domain has not been reported (Motchoulski and Liscum, 1999, Roberts et al., 2011).

There are 33 NRL gene family members in Arabidopsis thaliana, including NPH3 and RPT2, but their functions are not limited to physiological activities such as plant phototropism, represented by NPH3 and RPT2 (Pedmale et al., 2010). AtNRL31 (AtNCH1/AtSR1P1) is involved in auxin-independent chloroplast accumulation and is also a positive regulator of plant immunity (Zhang et al., 2014, Suetsugu et al., 2016). AtNRL6 (AtNYP2), AtNRL7 (AtNYP4), AtNRL20 (AtMAB4/ENP/NPY1), AtNRL21 (AtNYP5) and AtNRL30 has functional redundancy in coordination with AGC kinase (cAMP-dependent protein kinase A, cGMP-dependent protein kinase G and phospholipid-dependent protein kinase C) in regulating auxin transport in organogenesis and root gravity response (Cheng et al., 2008, Li et al., 2011). AtNRL8 (AtSETH6) is involved in the regulation of pollen germination and pollen tube growth, while AtNRL23 (AtDOT3) is related to vein structure regulation pattern formation, vascular system development and reproductive development (Lalanne et al., 2004, Petricka et al., 2008). The study of AtNPH3 homologous gene CPT1 (COLEOPTILE PHOTOTROPISM 1) in rice showed that CPT1-mediated coleoptile phototropism was achieved by auxin lateral transport and subsequent growth redistribution (Haga et al., 2005). After overexpression of WIN1 (WINDING 1) gene in rice, the helical phenotype and auxin were unevenly distributed in seedlings. Exogenous application of auxin polar transport inhibitor did not affect the helical phenotype, and overexpression of WIN1 did not affect the phototropism (Cheng et al., 2017). SlBTB5, a member of NRL gene family in tomato cultivar M82, is highly expressed in roots and flowers and down-regulated under environmental stress. StNRL1, a member of NRL gene family in potato, is a sensitive factor in plant immunity caused by potato late blight and participates in plant immune regulation (Yang et al., 2016, Li et al., 2018). NRL gene family members are widely involved in plant growth and development and stress response. However, the function of this gene family member, especially in monocotyledonous plants, remains to be further studied.

At present, there are few studies on NRL gene family, only in Arabidopsis thaliana, while the whole genome analysis of NRL gene family in rice has not been reported. In this study, rice NRL gene family members were screened and analyzed by bioinformatics methods to provide reference and basis for further study of rice NRL gene family.

1 Results and Analysis

1.1 Identification of NRL gene family in rice

In this study, 30 rice NRL family genes were obtained by local BLAST and HMMER analysis methods, and the predicted rice NRL family genes were screened by NCBI online tool Batch CD-Search (https://www.ncbi.nlm.nih.gov/cdd/), SMART (http://smart.embl-heidelberg.de/), and Pfam (http://pfam.xfam.org/). A total of 27 rice NRL family genes were identified and named as OsNRL1~OsNRL27 (Table 1). The length of CDS of rice NRL family genes ranged from 924 bp to 2 289 bp, and the amino acid sequence length ranged from 307 to 762. The predicted molecular weight of the protein was between 31.37~80.62 kD, and the theoretical isoelectric point was between 4.66~10.21. The NRL gene family members in rice were predicted to locate in the cytomembrane, cytoplasm, nucleus, plastid, peroxisome and endoplasm. In which, eleven NRL gene family members were predicted to locate in the nucleus, and six NRL gene family members were predicted to locate in the cytomembrane.

1.2 Chromosome distribution and gene duplication analysis of NRL gene family in rice

The location information of rice NRL family genes were obtained from RGAP (Rice genome annotation project) (http://rice.plantbiology.msu.edu/), and the chromosome distribution map of rice NRL family genes was drawn by TBtools software (Figure 1). The 27 rice NRL family genes were unevenly distributed on rice chromosomes except chromosome 10. Among them, the NRL genes on chromosome 3 were the most, with a total of seven genes, while only one NRL gene was distributed on chromosomes 5, 6 and 8, respectively.

MCScanX software was used to analyze rice tandem duplication events and whole genome duplication (WGD) or segmental duplication events. A total of seven gene duplication events occurred in the NRL gene family of rice, including two tandem duplication events and five WGD or segmental duplication events (Figure 1; Table 2). Gene pairs OsNRL22-OsNRL23 and OsNRL24-OsNRL25 were tandem replication, while gene pairs OsNRL1-OsNRL15, OsNRL4-OsNRL12, OsNRL22-OsNRL24, OsNRL26-OsNRL8 and OsNRL27-OsNRL9 were WGD or segmental duplication. DnaSP 6.0 software was used to calculate the Ka/Ks values of duplication gene pairs to evaluate the driving force of NRL gene evolution in rice. Ka/Ks > 1 means positive selection, Ka/Ks < 1 means purification selection, Ka/Ks = 1 means neutral selection. The Ka/Ks values of duplication gene pairs events in rice NRL family genes ranged from 0.107 0 to 0.546 5, indicating that they were purifying selection during evolution (Table 2).

1.3 Phylogenetic analysis of NRL gene family in rice

In order to further clarify the NRL gene family in rice, the protein sequences of dicotyledon Arabidopsis, grape and tomato, monocotyledon maize, barley, and Brachypodium were obtained from the online database Phytozome (https://phytozome.jgi.doe.gov/pz/portal.html), and 33, 24, 27, 31, 26 and 24 NRL gene family members were identified, respectively, and the phylogenetic relationship was analyzed (Figure 2). The results showed that there were 192 members of NRL gene family in seven species, which could be divided into six groups (Group Ⅰ~Ⅵ) with 8, 23, 42, 39, 54 and 26 members, respectively. OsNRL3 (OsCPT1) in Group VI is homologous to AtNPH3, which is consistent with previous reports (Haga et al., 2005). In Group VI, there are two genes in maize and tomato that had similar evolutionary relationships with OsNRL3 (OsCPT1) and AtNPH3, that is, Zm00001d004440, Zm00001d016898, Solyc01g105680 and Solyc10g047530. While only HORVU6Hr1G015480, Bradi3g46480 and VIT_203s0038g00270 are homologous genes of OsNRL3 (OsCPT1) and AtNPH3 in barley, Brachypodium and grape, respectively (Figure 2). In Group IV, OsNRL22, OsNRL24 and Zm00001d005051, Zm00001d023314 are homologous genes of AtRPT2, while the homologous genes of AtRPT2 in barley, Brachypodium, tomato and grape are HORVU4Hr1G023260, Bradi4g25900, Solyc07g043130 and VIT_206s0004g08230, respectively. Group V contains 54 NRL gene family members, which is the largest group of NRL gene family members. There are 8 NRL gene family members in Arabidopsis and rice, among which AtNRL6, AtNRL7, AtNRL20, AtNRL21 and AtNRL30 have functional redundancy (Cheng et al., 2008, Li et al., 2011).

1.4 Genetic structure and conserved motif analysis of NRL family in rice

The results of genetic structure analysis of NRL family in rice showed that there were 4 exons and 3 introns in 17 rice NRL family genes, such as OsNRL18, OsNRL7, OsNRL11 and OsNRL20. 5 rice NRL family genes contained 3 exons and 2 introns, that was, OsNRL10, OsNRL14, OsNRL17, OsNRL22 and OsNRL24. 2 rice NRL family genes contained 5 exons and 4 introns, that was, OsNRL3 and OsNRL6. While OsNRL15 contained 2 exons and 1 intron, OsNRL1 contained 1 intron. OsNRL20 contained the largest number of exons/introns, with 6 exons and 5 introns (Figure 3B). Further conserved motif analysis showed that most rice NRL family members contained 14~15 conserved motifs (Figure 3C). The BTB domain was predicted to be composed of N-terminal motifs 2, 4 and 6, N-terminal motifs 1, 3, 5 ,7, 10, 11 and 14 were predicted to be composed of NPH3 domain, and C-terminal motif 13 was predicted to be composed of coiled-coil domain. Both BTB domain and coiled-coil domain can be involved in protein interaction. The absence of any domain may affect the interaction with potential specific proteins, while the specific function of NPH3 domain remains to be further studied (Motchoulski and Liscum, 1999, Inada et al., 2004, Roberts et al., 2011).

1.5 Expression analysis of NRL gene family in rice

To further analyze the expression characteristics of rice NRL family genes in different tissues, we obtained RNA-Seq data of ten different tissues from RGAP (Rice genome annotation project) (http://rice.plantbiology.msu.edu/) and performed hierarchical clustering analysis on the expression data of rice NRL family genes (Figure 4). The data showed that NRL family genes in rice were expressed in different degrees in different rice tissues, and they could be divided into four groups according to the clustering analysis results. There were 7, 13, 4 and 3 genes in the first group to the fourth group, respectively (Figure 4). Genes in the first group, namely OsNRL7, OsNRL8, OsNRL14, OsNRL16, OsNRL17, OsNRL19 and OsNRL21, were highly expressed in inflorescences and pistils before heading, and the expression levels of OsNRL7 and OsNRL14 were also high in seed-5 days after pollination. In the second group, 13 NRL family genes were highly expressed in the inflorescence before heading, and OsNRL23, OsNRL25 and OsNRL26 were also highly expressed in the leaves. OsNRL20 was also highly expressed in the inflorescence after heading. In the third group, OsNRL6, OsNRL12, OsNRL22 and OsNRL24 were highly expressed in leaves, while in the fourth group, OsNRL2, OsNRL13 and OsNRL18 were highly expressed in inflorescence and anther after heading. It is worth noting that some duplication genes, such as OsNRL22 and OsNRL24, are clustered in the same group, suggesting that some WGD or segmental duplication genes have the same or similar expression regulation sequences and have similar expression regulation patterns. Therefore, the expression of duplication genes is further analyzed globally.

Microarray data were used to analyze the expression patterns of WGD or segmental duplication gene pairs and tandem duplication gene pairs of NRL gene family in rice. The lack of partial expression data of OsNRL1 and OsNRL15, OsNRL27 and OsNRL9 gene pairs was not included in the analysis (Figure 5). The tandem duplication genes of OsNRL22 and OsNRL23, OsNRL24 and OsNRL25 showed different expression patterns. The WGD or segmental duplication genes of OsNRL4 and OsNRL12, OsNRL22 and OsNRL24, OsNRL26 and OsNRL8 showed similar expression patterns, respectively.

2 Discussion

NRL (NPH3/RPT2-Like) gene family is plant-specific. The functions of 10 members of 33 gene families in Arabidopsis thaliana, including NPH3 and RPT2, have been identified (Christie et al., 2018). It is believed that the NRL gene family is involved in the regulation of auxin-dependent and auxin-independent physiological responses mediated by members (such as phototropinphot1 and phot2) of the VIIIsubfamily of AGC kinases (Suetsugu et al., 2016, Christie et al., 2018). Only two members of NRL gene family, CPT1 and WIN1, were identified in rice. CPT1 has been proved to be involved in the phototropism of coleoptile and the lateral transport of auxin, while WIN1 is related to auxin transport, but does not participate in the phototropism of coleoptile and root (Haga et al., 2005, Cheng et al., 2017).

In this study, 27 NRL family genes were identified from rice genome by bioinformatics methods, and two NRL family genes, namely OsNRL1 and OsNRL15, were added compared with previous reports (Gingerich et al., 2007). Compared with other rice NRL family genes, OsNRL1 and OsNRL15 have fewer exon/intron structures and shorter amino acid sequences, suggesting that they may be pseudogenes. However, unlike the general pseudogenes that are lower than homologous genes, the expression of OsNRL1 and OsNRL15 in many tissues is not lower than that of their homologous genes OsNRL3 (OsCPT1) (Zou et al., 2009). Therefore, to determine whether OsNRL1 and OsNRL15 are pseudogenes needs to be combined with the results of future gene functional studies.

In this study, 27 rice NRL family genes were unevenly distributed on 12 chromosomes, and there were some duplication gene pairs, that is, 5 WGD or segmental duplication gene pairs and 2 tandem duplication gene pairs. Gene duplication is one of the driving forces of evolution, which is involved in the formation and functional differentiation of new genes, and there may be functional redundancy duplication genes (Panchy et al., 2016). It has been reported that tandem duplication and WGD or segmental replication play a major role in the expansion of a single gene family (Kong et al., 2019). In this study, there were seven gene duplication events in the rice NRL gene family, indicating that gene duplication played an important role in the gene expansion of the rice NRL gene family, and WGD or segmental duplication played a more important role than tandem duplication. In the phylogenetic relationship analysis, the members of the NRL gene family of seven species, including rice, can be divided into six groups (Christie et al., 2018). AtNPH3 and AtRPT2 were in Group VI and Group IV, respectively. The rice homologous gene OsNRL3 (OsCPT1) in the same group with AtNPH3 was also involved in the phototropism response, and the rice homologous genes OsNRL22 and OsNRL24 in the same group with AtRPT2 were not reported (Haga et al., 2005). AtNPH3 and AtRPT2 have seven and six homologous genes in the other five species, respectively, and these homologous genes may be similar to the function of OsNRL3 (OsCPT1), and also participate in phototropism and other physiological responses of plants mediated by phototropism.

In this study, it was found that rice NRL family genes were expressed in many tissues, and some genes were highly expressed in some tissues, such as leaves, inflorescences before and after heading, anthers and pistils. OsNRL3 (OsCPT1) is the first reported rice NRL family gene, which makes the phototropism of rice coleoptile nearly disappear completely after mutation (Haga et al., 2005). OsNRL3 (OsCPT1) was highly expressed in inflorescence before heading and pistils, indicating that OsNRL3 (OsCPT1) may also play a role in rice reproductive development. For OsNRL7 (OsWIN1), on the one hand, the seedlings of its overexpressed strain WIN1-OX showed helical phenotype, while the coleoptile of this line and the T-DNA insertion mutant line WIN1_Act showed normal phototropism response, indicating that some of the genes represented by OsNRL7 (OsWIN1) in rice NRL family genes may have functional specificity. On the other hand, the seed size of the two lines was smaller than that of wild type seeds. However, OsNRL7 (OsWIN1) was expressed in many rice tissues including seeds and embryos, indicating that OsNRL7 (OsWIN1) may be involved in the regulation of rice seed size (Cheng et al., 2017). Combined with tissue expression analysis and evolutionary relationship analysis, it was found that genes similar to OsNRL3 (OsCPT1), namely OsNRL1 and OsNRL15, and OsNRL7 (OsWIN1), which are OsNRL6, OsNRL7, OsNRL22, OsNRL23, OsNRL24 and OsNRL25 in rice NRL family genes may play a role in physiological activities such as phototropism and auxin transport in plants. In addition, from the RNA-Seq and microarray expression data, it can be seen that the expression patterns in the WGD or segmental duplication genomes of OsNRL4 and OsNRL12, OsNRL22 and OsNRL24, OsNRL26 and OsNRL8 are similar, especially the expression patterns of OsNRL22 and OsNRL24 duplication gene pairs are basically the same, and both of them are highly expressed in leaves, indicating that the composition of cis-acting elements in their promoter regions may be similar and their functions as well. The possible functional redundancy should be considered in their research.

3 Materials and Methods

3.1 Identification of NRL gene family members in rice

The MSU 7.0 version of rice genome information was downloaded from the RGAP (http://rice.plantbiology.msu.edu/). HMM (Hidden markov model) (PF03000) of NPH3 domain and HMM (PF00651) of BTB domain were obtained from Pfam (http://pfam.xfam.org/). HMM and HMMER 3.0 software were used to perform the local HMM SEARCH on rice protein sequences to predict NRL family genes, and the E value was less than 1×10^-10. At the same time, BLAST 2.9.0 software was used for local BLASTP search, and the E value was less than 1×10^-10. Combined with the two results, a total of 30 possible members of rice NRL gene family were identified. The predicted rice NRL family genes were screened by NCBI online tool Batch CD-Search (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi), SMART (http://smart.embl-heidelberg.de/) and Pfam, and 27 NRL genes were identified as rice NRL family by removing genes with predicted domain length less than NPH3 domain or 50% of BTB domain. Gene information of NRL family genes was obtained from RGAP (http://rice.plantbiology.msu.edu/) (Huang et al., 2015; Chen et al., 2017). Plant-mSubP (http://bioinfo.usu.edu/Plant-mSubP/) was used for the prediction of protein subcellular localization.

3.2 Chromosome distribution and gene duplication analysis of NRL gene family in rice

The position information of genes on chromosomes in rice was obtained by RGAP (http://rice.plantbiology.msu.edu/), and the chromosome distribution information of NRL gene family in rice was screened out. MCScanX software was used to analyze the gene duplication events in rice, and the gene duplication pairs in rice NRL gene family were screened and extracted. The chromosome distribution and gene duplication diagram of rice NRL gene were drawn by TBtools software (Chen et al., 2020). Ka/Ks (Nonsynonymous substitution rates/Synonymous substitution rates) was calculated with the help of DnaSP 6.0 software. And the selection pressure of duplication gene pairs was analyzed.

3.3 Phylogenetic analysis of NRL gene family

Identification of NRL gene family members for the obtained protein sequences of dicotyledons (A. thaliana, grape, tomato) and monocotyledons (maize, barley, Brachypodium) was performed with the help of online database Phytozome (https://phytozome.jgi.doe.gov/pz/portal.html). The neighbor-joining method was used to analyze the phylogenetic relationship of NRL gene family members by MEGA 7.0. In which, the model was set to Poisson model, Bootstrap was set to 1000, and the phylogenetic tree was drawn by online tool Evolview v2 (http://nar.oxfordjournals.org/content/44/W1/W236) at the same time. Using the IQ-tree component of TBtools software, the phylogenetic tree of rice NRL gene family was constructed by maximum likelihood method, with Bootstrap set to 1000 (Chen et al., 2020).

3.4 Analysis of NRL family gene structure and conserved motif in rice

Structure analysis of NRL gene family members in rice was performed with the help of the online website CSDS 2.0 (http://gsds.cbi.pku.edu.cn/). Conserved motif analysis of NRL gene family members in rice was performed with the help of the online website MEME (http://meme-suite.org/tools/meme), with default parameter and 15 motifs. And the conserved motif diagram was completed by software TBtools (Chen et al., 2020).

3.5 Expression analysis of NRL gene family in rice

The expression data of different rice tissues were downloaded from the RGAP (http://rice.plantbiology.msu.edu/). R language pheatmap was used to standardize the expression data of NRL family genes in rice by Z-score method, and hierarchical clustering analysis was carried out. The temporal and spatial expression microarray data (GSE21396) of various tissues/organs in rice during the whole growth process in the field obtained by NCBI Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo/) were used to analyze the expression pattern of duplication gene pairs in rice NRL family.

Authors’ Contributions

HYY was the experimental designer and executor of this research. HYY completed the data analysis and manuscript writing. SLL and WDX participated in the experimental design, results analysis, manuscript writing and revision. ZDB and CWG conceived of the study, guided the experimental design, data analysis, writing and revision. All authors read and approved the final manuscript.

Acknowledgments

This study was supported by the National Key R & D Program (2016YFD0100804), Agricultural Science and Technology Independent Innovation Fund of Jiangsu Province (JASTIF, CX(18)1001) and Science Foundation for Post Doctorate of China (Grant 2017M621451).

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