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Expression analyses of miRNA Up-MIR-843 and its target genes in Ulva prolifera
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Juanjuan Yang1, Dachun Yu1, Songdong Shen1, *
Acta Oceanologica Sinica | 2020, 39(10) : 27 - 34
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Acta Oceanologica Sinica | 2020, 39(10): 27-34
• Recent Research on the Yellow Sea Green Tide Caused by Ulva prolifera •
Expression analyses of miRNA Up-MIR-843 and its target genes in Ulva prolifera
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Juanjuan Yang1, Dachun Yu1, Songdong Shen1, *
Affiliations
  • 1 Department of Cell Biology, School of Biology and Basic Medical, Soochow University, Suzhou 215123, China
Published: 2020-10-25 doi: 10.1007/s13131-020-1657-2
Outline
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microRNAs (miRNA) families play a critical role in plant growth, development, and responses to abiotic stress. In this study, we characterized Up-miR-843 and its targets genes in Ulva prolifera responses to nitrogen depravation and heat stress. The data demonstrated that 184 target genes of Up-miR-843 could be successfully validated. N deficiency not heat stress stimulus induced increase in abundance of the Up-miR-843 while exhibited reverse expression of target genes, including cyclin A3 and cyclin L, which were strictly required for cell cycle progression. In addition, U. prolifera with highly expression of Up-miR-843 showed improved biomass, and photosynthesis compared with that under normal growth conditions. Thus, the N deprivation and heat responsive miRNAs might be a possible member mediating the expression of these target genes, which further regulated the growth of U. prolifera.

cyclins  /  nitrogen deprivation  /  microRNA  /  U. prolifera  /  heat stress
Juanjuan Yang, Dachun Yu, Songdong Shen. Expression analyses of miRNA Up-MIR-843 and its target genes in Ulva prolifera[J]. Acta Oceanologica Sinica, 2020 , 39 (10) : 27 -34 . DOI: 10.1007/s13131-020-1657-2
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1 Introduction
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Ulva prolifera is one of the most common bloom-forming macroalgae, which broken out since 2008 in the Yellow Sea (Lin et al., 2011) and have caused both ecological and economic impacts to coastal environments and human activities. These blooms of opportunistic macroalgae are generally explained by eutrophication caused by the increased nutrient (Conley et al., 2009; Pérez-Mayorga et al., 2011), optimal light, temperature and so on (McGlathery, 2001; Taylor et al., 2001).
While physical forcing by winds and tides in shallow estuaries can lead to the rapid replacement of more saline, nutrient-poor marine water, higher surrounding temperature (Stumpf et al., 1993), Ulva still exhibited rapid nutrient uptake and subsequent growth. For example, U. lettuce maintained the ability to take up ammonium and nitrate under conditions of rapidly changing salinity (Lartigue et al., 2003), and nitrogen would be the limiting for the growth of U. curvata only at saturated light conditions (Coutinho and Zingmark, 1993). Therefore, we hold the view that Ulva might evolve self-regulating mechanisms to adapt to this abiotic stress.
miRNAs are a group of the non-coding small RNA, which play vital roles in mediating plant growth, development, abiotic stress adaptation and so on (Jones-Rhoades et al., 2006; Voinnet, 2009). During past decade, various of the miRNAs that are involved in transducing nutrient signaling, including starvation of nitrogen (Gao et al., 2016; Paul et al., 2015) have been documented, for example, miR-395, miR-399 mediated the regulation of sulfate and phosphate homeostasis, respectively (Chiou et al., 2006; Liang et al., 2010); and miR-169 oppositely regulated N starvation response via target NFYA (nuclear factor Y, subunit A) in Arabidopsis thaliana (Zhao et al., 2011). In addition, the small RNA-sequencing methods suggested that elevated temperature can alter the expression of miR-156/miR-157 and miR-172, mediating the growth and development of Arabidopsis (May et al., 2013), miR-396 protected sunflower from high-temperature stress via post-transcriptionally regulation of HaWRKY6 (Giacomelli et al., 2012). Therefore, it is safe to presume that plant cells must be capable of sensors (protein or other macromolecules) to adapt to the changes, while there has been less previous evidence for how these sensors participate in mediating development of U. prolifera adaptation to abiotic stress. In this study, we verified expression of miRNAs under N limitation or heat stress conditions based on the constructed small U. prolifera thalli RNA library (Huang et al., 2011), and investigated the changes of the candidate target genes, which may help elucidate the complex mechanisms as to how U. prolifera tolerate theses stressors.
2 Materials and methods
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2.1 Alga culture and treatments
Floating U. prolifera was gifted by Jiacheng Li from Zhejiang University, China. The algal was cultured at 20°C in SPX-GB-250 intelligent illumination incubators (Botai, Shanghai, China) for 4 d in fresh distilled seawater. Then U. prolifera was cultured in prepared cultural medium, which was made up as reported (Breuer et al., 2012).
Light was provided by a halogen lamp at PAR of 100 μmol/(m·s) and light time was 12 h. The culture medium was renewed every day, temperature stress experiments were performed after pretreatment, and 36°C was set as the heat stress conditions.
2.2 Determination of growth rates and contents of chlorophylls
Approximately 0.1 g algal was cultured under the pre- or N-culture medium at 20°C, or in the pre-culture medium at 36°C in the incubators and at the indicated time points, the algal material was reweighed.
For chlorophylls detection, samples were ground in liquid nitrogen, suspended in extraction buffer (80% (v/v) acetone). After incubation on ice for 15 min, the samples were centrifuged at 6 000 r/min for 10 min at 4°C. Concentration (c) of chlorophylls (a, b) was determined according to the methods described by Arnon (1949). The equations were used as following:
cChl a = (12.71 × A663 – 2.59 × A645) × V / (W × 1 000),
cChl b = (22.88 × A645 – 4.67 × A663) × V / (W × 1 000),
where V represents the volumes of extraction buffer, and W represents the weight of algae samples used.
2.3 Gene expression analysis
Ulva prolifera was harvested at different time point and grinded in liquid nitrogen. RNA was extracted using TRIzol reagents (Thermo Fisher Scientific, Waltham, MA, USA), and total 2 μg RNA was reversed using HifairTM Ⅱ 1st Strand cDNA Synthesis Kit (Yeasen, China). For miRNA detection, total 2 μg RNA was reversed using miRNA First Strand cDNA Synthesis (Sangon Biotech, China). Then the expression of genes was detected through Applied BiosystemsTM PowerTM SYBRTM Green Mix (Thermo Fisher Scientific) and calculated as described by Liao et al. (2017). The specific primer pairs used for qRT-PCR are listed in Table 1, 18S rRNA and U4 snoRNA were used as internal controls for mRNA and miRNAs, respectively. All tests were made for three times in a same way with independent sample data.
2.4 Identification of the Up-MIR-843 target genes
To characterize the target genes interacted with Up-MIR-843, an online tool referred to as psRNATarget (Plant microRNA Potential Target Finder; http://plant grn.noble.org/psRNA Target/) was run to scan against cDNA databases using the mature Up-MIR-843 sequence as query. Since the cDNA database for U. prolifera was not totally published, the similar cDNA library used for prediction contained Arabidopsis thaliana, transcript, JGI genomic project, Phytozome 11, 167 TAIR10. The target gene functions were defined based on BLASTx search results in NCBI (https://www. ncbi. nlm. nih. gov/).
2.5 Statistical analysis
The mean SE of the three independent experiments was considered as each value. All data were analyzed by SPSS 20.0 (Windows, USA). Use Duncan’s test and ANOVA to determine significance. A probability level of 5% (P< 0.05) was regarded as statistically significant.
3 Results
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3.1 Effect of temperature and N starvation on the growth of U. prolifera
To verify the effect of abiotic stress on the growth of U. prolifera, algal was cultured under different conditions, the weight of which was weighed every day. The results demonstrated that compared with normal culture condition, the weight of U. prolifera maintained stability over heat or N deprivation stress, however, U. prolifera had notably decreased chlorophyll a and chlorophyll b contents exposure to N starvation condition not to heat stress (Fig. 1).
3.2 Up-miR-843 was conversed across green algae and embryophyte
Based on the sole published constructed and sequenced small RNA libraries from U. prolifera (Huang et al., 2011), firstly we verified expression of miRNAs using qRT-PCR assay, and miRNAs within count less than 500 were excluded in the study. The chosen miRNAs were identified to search the homologues in miRbase database (http://www.mirbase.org/search.shtml). As shown in Table 2, among the 60 candidate miRNAs, only 13 miRNAs matched the corresponding other plant miRNAs. The homologs of miR-1048, miR-2119, miR-2679, miR-2916 and miR-390 in U. prolifera were found in Physcomitrella patens, Glycine max, Medicago truncatula, Populus euphratica, respectively. miR-3911 and miR-3519 matched the homologs in Arachis hypogaea. Five miRNAs homologs, miR-443, miR-827, miR-1858, miR-1874, and miR-1877 were found in Oryza sativa.
Among these identical miRNAs, the mature sequence of Up-miR-843 is 19 nt-long in length (5’-TTTAGGTAGAGCCTCATGA-3’), which was identified to be identical to Ath-miR-843 (Fig. 2), which suggested that the miR-843 members may be conserved across green algal and embryophyte.
3.3 Up-miR-843 targets different genes functional in various biological process
Based on running an online tool (http://plantgrn.noble.org/psRNATarget/), the genes putatively targeted by miRNAs were predicted. Results indicated that totally 184 genes (including some genes encoding proteins unknown) were interacted by this U. prolifera miRNA, whilst genomic database for U. prolifera was still unpublished, so we used Arabidopsis thaliana cDNA database as cardiant target library. The target genes with the accurate annotation were as shown in Table 3, which contains genes encoding calmodulin-binding receptor-like cytoplasmic kinase 3, NIMA-related kinase 7, Protein phosphatase 2A regulatory B subunit family protein, peptide-N-glycanase 1, F-box and associated interaction domains-containing protein, Cyclin family protein and so on. Among which, we chose cyclins as the cardiants basing on the RNA-seq previously reported (He et al., 2018) before. Table 4 indicated all the cyclins in the U. prolifera.
3.4 Up-miR-843 and its target genes under abiotic stress
Expression patterns of Up-miR-843 and its target genes upon N starvation or high temperature stress were investigated in more detail. Results indicated Up-miR-843 showed down-regulated transcripts abundance after 12 h, while all target genes displayed reverse expression patterns to miRNAs upon N starvation, such as upregulated cyclin A3 expression over 24 h whilst increased levels of cyclin L over 12 h, the promoted transcripts under stresses were gradually repressed along the exposed time (Fig. 3). Therefore, Up-miR-843 regulates the target genes post-transcriptionally and establishes putative miRNA/target modules that mediate plant nitrogen starvation and high temperature stimulus.
4 Discussion
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To our knowledge, abiotic stress conditions such as extreme temperature, salinity, nutrient deprivation, would inhibit root development, photosynthesis, and further thereby causing the damage of the overall plant growth and productivity (Suzuki et al., 2014; Zhang, 2015). The mechanism underlying such responses results from the differential production of several transcripts and their associated proteins. As one class of post-transcriptional regulators of gene expression, microRNAs (miRNAs) have been proven to play a central role in many biological processes including organ development, phase transition, and abiotic stress tolerance (Hackenberg et al., 2015; Niu et al., 2016; Vidal et al., 2010; Bi et al., 2007). For instance, miR-169, miR-398a decreased in Arabidopsis seedlings, whereas pri-miR-156, miR-447c were induced under N limitation (Hsieh et al., 2009), and nine miRNA families (miR-160, miR-167, miR-168, miR-169, miR-319, miR-395, miR-399, miR-408, and miR-528) were identified to respond to low nitrogen in maize roots (Xu et al., 2011). In our study, we found that 12 h of N limitation decreased the levels of U. prolifera miRNA (Up-miR-843), whereas it was restored after 48 h exposure to nitrogen deficiency. Hence, this miRNA was identified to be identical to Arabidopsis Thaliana homolog miRNA (Ath-miR-843), indicating the miR-843 members are conserved across green algal and embryophyte. Furthermore, as previously reported, low levels of miR-843 contributed to the tolerance of plants to nutrient deficiencies (Lu et al., 2014), we also found N deficiency inhibited the expression of miR-843, which provided the evidence that Up-miR-843 might play an important role in the development of U. prolifera under nitrogen deficiency stimulus.
Expect for the nutrient deficiency mentioned above, temperature is also a critical factor controls plant growth and development (Patel and Franklin, 2009). For most plant species, heat stress induced protein denaturation (Hasanuzzaman et al., 2013), while U. prolifera started to proliferate followed the increased temperature from 9.9°C to 20.3°C (Wang et al., 2015), even maintained the stability of contents of chlorophylls and growth rates at 36°C, which is of interest to know whether U. prolifera developed unique adaptations. To our knowledge, temperature response connected non-coding RNAs has been observed in different plant species, such as heat stress induced the expression of mature-miR-160a, miR-166a in spring barley plants (Kruszka et al., 2014), and enhanced levels of miR-162b, miR-171b in Oryza sativa (Li et al., 2015). In this study, the decreased trends of miR-483 was found but no significant difference was verified, suggesting that U. prolifera could burden heat stress more than other plants, and miRNAs might not the mediator in this process.
So why non-coding RNAs functioned differently in U. prolifera facing the N deficiency and heat stress stimulus, respectively. A total of 184 target genes of Up-miR-843 was identified as the effectors, especially two cyclins families. Hence, based on the transcriptome sequencing studies in our laboratory (He et al., 2018), we demonstrated that cyclin U4, L, A2, C, A3 in U. prolifera shared the differently similarity with Selaginella moellendorffii, Brassica napus, Aphis gossypii, Brachypodium distachyon and Arabidopsis thaliana, respectively, which is consistent with the cyclins family members in other plants (Mironov et al., 1999). However, only expression of cyclin L, A3 could be detected using qRT-PCR analysis in this study, which suggested cyclin L, A3 may be the two conversed cyclin genes during the evolution of plants. As previous report mentioned, the steady-state levels of cyclin A RNAs increased at or after the onset of S phase till G2 and occasionally M phases, and cyclin B RNAs only present in G2 and M phases (Ferreira et al., 1994; Kouchi et al., 1995; Meskiene et al., 1995), especially cyclin A3 genes occurred earlier in S phase (Reichheld et al., 1996), similarly, 24 h of N starvation not heat stress induced the expression of cyclin A3 and cyclin L. Based on the findings that cyclin L overexpressing could stimulate splicing and/or other steps of mRNA metabolism, further grant salt tolerance in Saccharomyces (Forment et al., 2002), we hold the hypothesis that miR-843 was a possible molecular mediating the expression of cyclin A3 and cyclin L, which reinforced the important regulatory function of alternative splicing for plant abiotic tolerance, however, the mediation function of miR-843 needed further study.
5 Conclusions
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In conclusion, we analyzed U. prolifera small RNA expression profiles and found
Up-miR-843 differentially expressed under N deficiency not heat stress stimulus. Hence, this abiotic-responsive miRNA targeted different transcription factors, among which both cyclin A3 and cyclin L functioned in stress response. Therefore, we hypothesized that miRNA might be a possible member mediating the expression of these selected genes in U. prolifera, and the function of this tiny non-coding RNA in complex biological networks needed further study.
Funding
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  • The National Key R&D Program of China under contract No. 2016YFC1402102; the project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
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Article Info
doi: 10.1007/s13131-020-1657-2
  • Receive Date：2019-09-11
  • Online Date：2026-03-31
  • Published：2020-10-25
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History
  • Received：2019-09-11
  • Accepted：2019-11-22
Funding
The National Key R&D Program of China under contract No. 2016YFC1402102; the project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Affiliations
    1 Department of Cell Biology, School of Biology and Basic Medical, Soochow University, Suzhou 215123, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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