Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (23): 4583-4599.doi: 10.3864/j.issn.0578-1752.2022.23.002


Identification of Wheat Circular RNAs Responsive to Drought Stress

LI Ning(),LIU Kun,LIU TongTong,SHI YuGang,WANG ShuGuang,YANG JinWen*(),SUN DaiZhen*()   

  1. College of Agriculture, Shanxi Agricultural University, Taigu 030801, Shanxi
  • Received:2022-07-25 Accepted:2022-09-05 Online:2022-12-01 Published:2022-12-06
  • Contact: JinWen YANG,DaiZhen SUN;;


【Objective】 Drought is one of the foremost abiotic stress limiting global wheat production. Exploring the molecular mechanism of wheat response to drought stress have great significance in wheat molecular breeding. Circular RNAs (circRNAs) have been proved to play an important role in the process of plants tolerance to environmental stresses. Therefore, identifying circRNAs involved in drought stress response will help to construct a regulatory network of wheat drought tolerance, and lay a foundation for analyzing the drought resistance mechanism in wheat. 【Method】 In this study, two wheat varieties (Zhoumai13 and Jimai38) with significant differences in drought resistance were used and circRNA-seq was performed on their root samples under well-watered and drought conditions. Differentially expressed circRNAs related to drought stress response were screened based on the identified circRNAs and their microRNAs (miRNAs) targets were predicted. Further, potential circRNA-miRNA-mRNA regulatory modules related to wheat drought stress response were constructed according to the expression patterns of miRNAs and their target genes under drought stress..【Result】 A total of 1 409 wheat circRNAs were identified, most of which (68.91%) were exonic circRNAs. Only 133 circRNAs were simultaneously identified in both varieties. A total of 239 differentially expressed circRNAs were identified under drought stress, of which 138 circRNAs were specifically differentially expressed in the drought-resistant variety Zhoumai 13 (ZM13), and 19 circRNAs were differentially expressed simultaneously in both varieties. Besides, 34 targeted miRNAs and 1 408 miRNA target genes were predicted. Based on the expression patterns of these differentially expressed circRNAs, targeted miRNAs, and miRNA target genes, five potential circRNA-miRNA-mRNA regulatory modules centered on tae-miR9664-3p, tae-miR1122b-3p, tae-miR9662a-3p, tae-miR6197-5p and tae-miR1120c-5p in response to drought stress were screened..【Conclusion】 Wheat circRNAs have obvious specificity in different cultivars and different expression patterns among different drought-tolerant wheat cultivars. A total of 239 wheat circRNAs and 5 potential circRNA-miRNA-mRNA regulatory modules in response to drought stress were identified in the present study.

Key words: wheat, circular RNAs, drought stress, microRNAs

Table 1

Primer sequences of real-time fluorescence quantitative PCR"

circRNA ID 正向引物 Forward primer (5′-3′) 反向引物 Reverse primer (5′-3′)

Table 2

Statistic of evaluating the circRNA-seq data"

Sample ID
Clean read数量
No. of clean reads
Clean data总碱基数
No. of bases in clean data
Percentage of mapped reads (%)
JM38-CK-1 118952370 17735106554 93.08 99.68
JM38-CK-2 116572800 17380371520 93.19 99.47
JM38-CK-3 120557430 17933660922 93.60 99.61
JM38-T-1 97797440 14495476172 94.01 98.74
JM38-T-2 115322786 17223097988 94.79 99.55
JM38-T-3 101091222 15052976916 93.24 99.47
ZM13-CK-1 109456900 16361760332 95.37 99.79
ZM13-CK-2 158882218 23410171332 94.23 99.32
ZM13-CK-3 129129306 19198145718 93.53 99.40
ZM13-T-1 120213128 17925334142 93.34 99.52
ZM13-T-2 106276928 15847825216 93.01 99.59
ZM13-T-3 119369138 17788551356 93.18 99.65

Fig. 1

Characterization of wheat circRNAs A: Venn diagram showing the amount and distribution of circular RNAs in two varieties; B: Pie chart representing the amount and percentage of circular RNAs generated from exons, introns, and intergenic regions; C: Histogram showing the number of circRNAs detected in wheat chromosomes; D: Histogram showing the length range distribution of wheat circRNAs"

Fig. 2

Differential expression analysis of circRNAs in two varieties A: Venn diagram showing the amount and distribution of differentially expressed circulars RNAs in two varieties; B: The number of up-regulated circRNAs and down-regulated circRNAs in the two varieties; C: Heatmap of the expression of differentially expressed circRNAs in the two varieties and the number represents log2(Fold change) values"

Fig. 3

Validation of expression patterns of differentially expressed circRNAs"

Table 3

GO annotation of host genes of differentially expressed circRNAs in both varieties"

GO类别 GO category GO名称 GO name GO ID 宿主基因数量 No. of host genes
Biological process
代谢过程Metabolic process GO:0008152 5
细胞过程Cellular process GO:0009987 3
生物调节Biological regulation GO:0065007 2
Cellular component
细胞外区域Extracellular region GO:0005576 2
膜Membrane GO:0016020 2
膜组分Membrane part GO:0044425 2
Molecular function
结合Binding GO:0005488 2
催化活性Catalytic activity GO:0003824 2

Table 4

KEGG annotation of host genes of all differentially expressed circRNAs"

Name of the KEGG pathway
KEGG number
No. of host genes
Name of the KEGG pathway
KEGG number
No. of host genes
Plant-pathogen interaction
ko04626 9 内吞作用
ko04144 6
真核生物中的核糖体生物发生Ribosome biogenesis in eukaryotes ko03008 4 植物激素信号转导
Plant hormone signal transduction
ko04075 4
Phenylpropanoid biosynthesis
ko00940 4 过氧化物酶体
ko04146 4
ko03040 3 氧化磷酸化
Oxidative phosphorylation
ko00190 2
mRNA surveillance pathway
ko03015 2 RNA转运
RNA transport
ko03013 2
Glycerolipid metabolism
ko00561 2 鞘糖脂生物合成
Glycosphingolipid biosynthesis
ko00604 2

Fig. 4

GO annotation of host genes of differentially expressed circRNAs A: GO annotation of host genes of all differentially expressed circRNAs; B: GO annotation of host genes of differentially expressed circRNAs specifically in ZM13"

Table 5

KEGG annotation of host genes of differentially expressed circRNAs specifically in ZM13"

Name of the KEGG pathway
KEGG number
No. of host genes
Name of the KEGG pathway
KEGG number
No. of host genes
Plant-pathogen interaction
ko04626 5 内吞作用
ko04144 4
RNA转运RNA transport ko03013 2 过氧化物酶体Peroxisome ko04146 2
Oxidative phosphorylation
ko00190 2 mRNA监测途径
mRNA surveillance pathway
ko03015 2
剪切体Spliceosome ko03040 2

Table 6

KEGG annotation of host genes of differentially expressed circRNAs in both varieties"

Name of the KEGG pathway
KEGG number
Host genes
Differentially expressed circRNAs
剪切体Spliceosome ko03040 TraesCS4D02G214100 chr4D:367041574|367041924
真核生物中的核糖体生物发生Ribosome biogenesis in eukaryotes ko03008 TraesCS2B02G435400 chr2B:625556656|625557509
植物激素信号转导Plant hormone signal transduction ko04075 TraesCS4A02G446600 chr4A:714100537|714100686
苯丙烷生物合成Phenylpropanoid biosynthesis ko00940 TraesCS2B02G613900 chr2B:793034311|793034526
过氧化物酶体Peroxisome ko04146 TraesCS6D02G174600 chr6D:164766767|164767073
甘油磷脂代谢Glycerolipid metabolism ko00561 TraesCS5A02G157700 chr5A:337941529|337942323
氨基糖和核苷酸糖代谢Amino sugar and nucleotide sugar metabolism ko00520 TraesCS1A02G353400 chr1A:536974543|536974758

Table 7

Homologous genes of differentially expressed circRNA host genes in rice and their stress resistance functions"

Differentially expressed circRNAs
Host genes
Homologous genes in rice
Homologous gene function
chr2A:52664278|52664553 TraesCS2A02G099900 OsEIL2LOC_Os07g48630 耐盐Tolerant to salt stress[30]
chr1D:299577794|299577982 TraesCS1D02G214200 OsNRT1.1BLOC_Os10g40600 耐低氮Tolerant to low nitrogen stress[31]
chr3A:638334965|638335214 TraesCS3A02G390200 OsPUB15LOC_Os08g01900 耐盐Tolerant to salt stress[32]
chr3D:394765145|394765294 TraesCS3D02G285400 OsTT1LOC_Os03g26970 耐高温Tolerant to high temperature stress[33]
chr4B:606908755|606908957 TraesCS4B02G317200 OsPht1;2LOC_Os03g05640 耐低钾Tolerance to low potassium stress [34]
chr4D:41728977|41729938 TraesCS4D02G066700 OsHOS1LOC_Os03g52700 耐冷Tolerant to cold stress[35]
chr5B:17981442|17981743 TraesCS5B02G018700 OsASTOL1LOC_Os12g42980 耐砷Tolerant to arsenic stress[36]
chr6A:608632503|608632694 TraesCS6A02G396400 OsPP1aLOC_Os03g16110 耐盐Tolerant to salt stress[37]
chr7A:222784992|222785194 TraesCS7A02G245100 OsSAP11LOC_Os08g39450 耐盐和耐旱Tolerant to salt and drought stress[38]
OsSAP1LOC_Os09g31200 耐盐和耐旱Tolerant to salt and drought stress[39]

Table 8

Differentially expressed circRNAs and their target miRNAs"

circRNA ID 靶向miRNA <BOLD>T</BOLD>arget miRNAs
chr2B:56775826|56778058 tae-miR9778
chr7A:735704463|735710613 tae-miR9673-5p; tae-miR9661-5p
chr1B:642165761|642197014 tae-miR9664-3p; tae-miR1133; tae-miR1122b-3p
chr5D:543694782|543696753 tae-miR9662a-3p
chr1B:518799941|518803372 tae-miR1137a
chr1B:477404890|477416633 tae-miR1137a; tae-miR1133; tae-miR1122b-3p
chr5B:528574134|528588868 tae-miR1135; tae-miR1133; tae-miR1127a; tae-miR1122a; tae-miR9668-5p; tae-miR1127b-3p
chr2B:32870327|32874189 tae-miR1121; tae-miR6197-5p;tae-miR9653a-3p
chr5A:482358772|482427161 tae-miR1117; tae-miR1125
chr7B:68317992|68345006 tae-miR1117
chr3B:778404617|778442815 tae-miR1117; tae-miR1133; tae-miR1131; tae-miR1127a; tae-miR1120c-5p
chr2B:787486469|787538256 tae-miR5384-3p
chr3A:7907994|7923795 tae-miR1117; tae-miR5049-3p
chr2A:771191685|771242152 tae-miR1117; tae-miR7757-5p; tae-miR1131
chr6D:454657953|454748495 tae-miR1121; tae-miR5175-5p; tae-miR1118; tae-miR1130b-3p; tae-miR1120c-5p
chr7B:1308928|1352258 tae-miR1122c-3p; tae-miR1133; tae-miR1127a; tae-miR1122a; tae-miR1127b-3p
chr4A:668278340|668323672 tae-miR1131; tae-miR9673-5p
chr2B:16815429|16856732 tae-miR1117; tae-miR1139; tae-miR1118; tae-miR408
chr4D:65120787|65147651 tae-miR1117; tae-miR9664-3p; tae-miR7757-5p; tae-miR1127a; tae-miR1122a
chr6D:469968655|469986922 tae-miR7757-5p; tae-miR1133
chr3B:54538153|54591607 tae-miR5384-3p; tae-miR9659-3p
chr6B:265924545|265976740 tae-miR9674a-5p
chr7D:615903829|615904057 tae-miR1122c-3p; tae-miR1130b-3p; tae-miR1120b-3p
chr1A:589450964|589476548 tae-miR1121; tae-miR1122c-3p; tae-miR1133; tae-miR171b; tae-miR1130a; tae-miR1130b-3p; tae-miR1120b-3p

Fig. 5

Distribution and expression patterns of differentially expressed target miRNAs and differentially expressed target genes in two varieties A, B: Distribution of differentially expressed target miRNAs; C: Expression patterns of differentially expressed target miRNAs; D, E: Distribution of differentially expressed target genes; F: Expression patterns of differentially expressed target genes"

Table 9

circRNA-miRNA-mRNA regulatory modules"

Differentially expressed
Differentially expressed
target miRNAs
Target genes of differentially
expressed miRNA
Target gene functional annotation
1 chr1B:642165761|642197014
tae-miR9664-3p TraesCS5B02G405300 过氧化物酶Peroxidase
TraesCS5A02G141700 乙烯反应转录因子
Ethylene-responsive transcription factor
TraesCS5D02G084300 细胞色素P450 Cytochrome P450
TraesCS3D02G225900 细胞色素P450 Cytochrome P450
TraesCS3B02G256400 细胞色素P450 Cytochrome P450
TraesCS3A02G224900 钙依赖性蛋白激酶Calcium-dependent protein kinase
TraesCS3B02G254500 钙依赖性蛋白激酶Calcium-dependent protein kinase
TraesCS3D02G228700 钙依赖性蛋白激酶Calcium-dependent protein kinase
TraesCS4B02G365000 ABC转运体A家族成员
ABC transporter A family member
TraesCSU02G138200 ABC转运体A家族成员
ABC transporter A family member
2 chr1B:642165761|642197014
tae-miR1122b-3p TraesCS1A02G272100 丝氨酸/苏氨酸蛋白激酶Serine/threonine-protein kinase
TraesCS7B02G481100 E3 泛素蛋白连接酶E3 ubiquitin-protein ligase
TraesCS7B02G165100 E3 泛素蛋白连接酶E3 ubiquitin-protein ligase
TraesCS6D02G330500 谷氨酸受体Glutamate receptor
TraesCS6B02G281000 乙烯反应转录因子
Ethylene-responsive transcription factor
TraesCS7D02G416700 胆碱单加氧酶Choline monooxygenase
TraesCS1B02G138100 生长素反应蛋白Auxin-responsive protein
TraesCS2D02G404800 水通道蛋白Aquaporin
TraesCS3D02G258200 ABC转运体B家族成员
ABC transporter B family member
3 chr5D:543694782|543696753 tae-miR9662a-3p TraesCS7A02G218600 锌指蛋白Zinc finger protein
TraesCS7D02G220300 锌指蛋白Zinc finger protein
TraesCS7B02G125500 锌指蛋白Zinc finger protein
TraesCS5B02G526300 富含半胱氨酸的受体蛋白激酶
Cysteine-rich receptor-like protein kinase
4 chr2B:32870327|32874189 tae-miR6197-5p TraesCS4A02G193600 WRKY转录因子WRKY transcription factor
TraesCS1D02G276100 转录因子TGAL5 Transcription factor TGAL5
TraesCS4D02G056900 转录因子bHLH25 Transcription factor bHLH25
TraesCS4D02G273600 丝氨酸/苏氨酸蛋白激酶Serine/threonine-protein kinase
5 chr3B:778404617|778442815
tae-miR1120c-5p TraesCS4A02G119400 普遍胁迫蛋白Universal stress protein
TraesCS4B02G275000 丝氨酸/苏氨酸蛋白激酶Serine/threonine-protein kinase
TraesCS4D02G273600 丝氨酸/苏氨酸蛋白激酶Serine/threonine-protein kinase
TraesCS3A02G045200 富含半胱氨酸的受体蛋白激酶
Cysteine-rich receptor-like protein kinase
TraesCS7B02G298200 肉桂酰辅酶A还原酶Cinnamoyl-CoA reductase
TraesCS7D02G391800 肉桂酰辅酶A还原酶Cinnamoyl-CoA reductase
[1] AKRAM N A, WASEEM M, AMEEN R, ASHRAF M. Trehalose pretreatment induces drought tolerance in radish (Raphanus sativus L.) plants: Some key physio-biochemical traits. Acta Physiologiae Plantarum, 2016, 38(1): 3.
doi: 10.1007/s11738-015-2018-1
[2] JECK W R, SHARPLESS N E. Detecting and characterizing circular RNAs. Nature Biotechnology, 2014, 32(5): 453-461.
doi: 10.1038/nbt.2890 pmid: 24811520
[3] SALZMAN J. Circular RNA expression: Its potential regulation and function. Trends in Genetics, 2016, 32(5): 309-316.
doi: S0168-9525(16)00032-9 pmid: 27050930
[4] LI L, GUO J, CHEN Y, CHANG C, XU C. Comprehensive CircRNA expression profile and selection of key circRNAs during priming phase of rat liver regeneration. BMC Genomics, 2017, 18(1): 80.
doi: 10.1186/s12864-016-3476-6 pmid: 28086788
[5] ZHENG Q, BAO C, GUO W, LI S, CHEN J, CHEN B, LUO Y, LYU D, LI Y, SHI G. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nature Communications, 2016, 7: 11215.
doi: 10.1038/ncomms11215 pmid: 27050392
[6] WANG K, BO L, FANG L, WANG J X, LIU C Y, BING Z, ZHOU L Y, TENG S, MAN W, TAO Y.A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223. European Heart Journal, 2016, 37(33): 2602-2611.
doi: 10.1093/eurheartj/ehv713 pmid: 26802132
[7] LI Z, HUANG C, BAO C, CHEN L, LIN M, WANG X, ZHONG G, YU B, HU W, DAI L. Exon-intron circular RNAs regulate transcription in the nucleus. Nature Structural and Molecular Biology, 2015, 22: 256.
doi: 10.1038/nsmb.2959 pmid: 25664725
[8] WANG P L, BAO Y, YEE M C, BARRETT S P, HOGAN G J, OLSEN M N, DINNENY J R, BROWN P O, SALZMAN J. Circular RNA is expressed across the eukaryotic tree of life. PLoS ONE, 2014, 9(3): e90859.
doi: 10.1371/journal.pone.0090859
[9] YE C Y, CHEN L, LIU C, ZHU Q H, FAN L J. Widespread noncoding circular RNAs in plants. New Phytologist, 2015, 208(1): 88-95.
doi: 10.1111/nph.13585
[10] YIN J L, LIU M Y, MA D F, WU J W, LI S L, ZHU Y X, HAN B. Identification of circular RNAs and their targets during tomato fruit ripening. Postharvest Biology and Technology, 2018, 136: 90-98.
doi: 10.1016/j.postharvbio.2017.10.013
[11] ZHOU R, ZHU Y X, ZHAO J, FANG Z W, WANG S P, YIN J L, CHU Z H, MA D F. Transcriptome-wide identification and characterization of potato circular RNAs in response to Pectobacterium carotovorum subspecies Brasiliense infection. International Journal of Molecular Sciences, 2018, 19(1): 71.
doi: 10.3390/ijms19010071
[12] WANG Y, YANG M, WEI S, QIN F, ZHAO H, SUO B. Identification of circular RNAs and their targets in leaves of Triticum aestivum L. under dehydration stress. Frontiers in Plant Science, 2017, 7: 2024.
[13] ZHAO W, CHENG Y, ZHANG C, YOU Q, SHEN X, GUO W, JIAO Y. Genome-wide identification and characterization of circular RNAs by high throughput sequencing in soybean. Scientific Reports, 2017, 7(1): 5636.
doi: 10.1038/s41598-017-05922-9 pmid: 28717203
[14] WEI T, JIE Y, YAN H, LI F, ZHOU Q, WEI C, BENNETZEN J L. Circular RNA architecture and differentiation during leaf bud to young leaf development in tea (Camellia sinensis). Planta, 2018, 248(10): 1-13.
doi: 10.1007/s00425-018-2910-1
[15] DARBANI B, NOEPARVAR S, BORG S. Identification of circular RNAs from the parental genes involved in multiple aspects of cellular metabolism in barley. Frontiers in Plant Science, 2016, 7: 776.
doi: 10.3389/fpls.2016.00776 pmid: 27375638
[16] CHEN L, ZHANG P, FAN Y, LU Q, LI Q, YAN J, MUEHLBAUER G J, SCHNABLE P S, DAI M, LI L. Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. New Phytologist, 2018, 217(3): 3.
[17] TAN J, ZHOU Z, NIU Y, SUN X, DENG Z. Identification and functional characterization of tomato circrnas derived from genes involved in fruit pigment accumulation. Scientific Reports, 2017, 7: 8594.
doi: 10.1038/s41598-017-08806-0 pmid: 28819222
[18] CHENG J, ZHANG Y, LI Z, WANG T, ZHANG X, ZHENG B. A lariat-derived circular RNA is required for plant development in Arabidopsis. Science China Life Sciences, 2018, 61(2): 204-213.
doi: 10.1007/s11427-017-9182-3
[19] PAN T, SUN X, LIU Y, LI H, DENG G, LIN H, WANG S. Heat stress alters genome wide profiles of circular RNAs in Arabidopsis. Plant Molecular Biology, 2018, 96(3): 217-229.
doi: 10.1007/s11103-017-0684-7
[20] LI N, LIU T T, GUO F, YANG J W, SHI Y G, WANG S G, SUN D Z. Identification of long non-coding RNA-microRNA-mRNA regulatory modules and their potential roles in drought stress response in wheat (Triticum aestivum L.). Frontiers in Plant Science, 2022, 10: 1011064.
[21] QUAN X, ZENG J, YE L, CHEN G, HAN Z, SHAH J, ZHANG G. Transcriptome profiling analysis for two Tibetan wild barley genotypes in responses to low nitrogen. BMC Plant Biology, 2016, 16(1): 30-45.
doi: 10.1186/s12870-016-0721-8
[22] SUN Y, SONG K, SUN L, QIN Q, JIANG T, JIANG Q, XUE Y. Morpho-Physiological and transcriptome analysis provide insights into the effects of zinc application on nitrogen accumulation and metabolism in wheat (Triticum aestivum L.). Plant Physiology and Biochemistry, 2020, 149: 111-120.
doi: 10.1016/j.plaphy.2020.01.038
[23] KIM D, LANGMEAD B, SALZBERG S L. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 2015, 12(4): 357-360.
doi: 10.1038/nmeth.3317 pmid: 25751142
[24] MEMCZAK S, JENS M, ELEFSINIOTI A, TORTI F, KRUEGER J, RYBAK A, MAIER L, MACKOWIAK S D, GREGERSEN L H, MUNSCHAUER M, LOEWER A, ZIEBOLD U, LANDTHALER M, KOCKS C, NOBLE F, RAJEWSKY N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 2013, 495(7441): 333-338.
doi: 10.1038/nature11928
[25] ZHU Y X, JIA J H, YANG L, XIA Y C, ZHANG H L, JIA J B, ZHOU R, NIE P Y, YIN J L, MA D F, LIU L C. Identification of cucumber circular RNAs responsive to salt stress. BMC Plant Biology, 2019, 19(1): 164.
doi: 10.1186/s12870-019-1712-3
[26] LOVE M I, HUBER W, ANDERS S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology, 2014, 15(12): 550.
doi: 10.1186/s13059-014-0550-8
[27] BO X, WANG S. Target Finder: A software for antisense oligonucleotide target site selection based on MAST and secondary structures of target mRNA. Bioinformatics, 2005, 21(8):1401.
doi: 10.1093/bioinformatics/bti211
[28] MA S W, WANG M, WU J H, GUO W L, CHEN Y M, LI G W, WANG Y P, SHI W M, XIA G M, FU D L, KANG Z S, NI F. WheatOmics: A platform combining multiple omics data to accelerate functional genomics studies in wheat. Molecular Plant, 2021, 14(12): 1965-1968.
doi: 10.1016/j.molp.2021.10.006 pmid: 34715393
[29] CONESA A, GÖTZ S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics, 2008, 2008: 619832.
[30] YANG C, LU X, MA B, CHEN S Y, ZHANG J S. Ethylene signaling in rice and Arabidopsis: Conserved and diverged aspects. Molecular Plant, 2015, 8(4): 495-505.
doi: 10.1016/j.molp.2015.01.003
[31] HU B, JIANG Z, WANG W, QIU Y, ZHANG Z, LIU Y, LI A, GAO X, LIU L, QIAN Y, HUANG X, YU F, KANG S, WANG Y, XIE J, CAO S, ZHANG L, WANG Y, XIE Q, KOPRIVA S, CHU C. Nitrate- NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nature Plants, 2019, 5(4): 401-413.
doi: 10.1038/s41477-019-0384-1
[32] PARK J J, YI J, YOON J, CHO L H, PING J, JEONG H J, CHO S K, KIM W T, AN G. OsPUB15, an E3 ubiquitin ligase, functions to reduce cellular oxidative stress during seedling establishment. The Plant Journal, 2011, 65(2): 194-205.
doi: 10.1111/j.1365-313X.2010.04416.x
[33] LI X M, CHAO D Y, WU Y, HUANG X H, CHEN K, CUI L G, SU L, YE W W, CHEN H, CHEN H C, DONG N Q, GUO T, SHI M, FENG Q, ZHANG P, HAN B, SHAN J X, GAO J P, LIN H X. Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nature Genetics, 2015, 47(7): 827-833.
doi: 10.1038/ng.3305
[34] AI P H, SUN S B, ZHAO J N, FAN X R, XIN W J, GUO Q, YU L, SHEN Q R, WU P, MILLER A J, XU G H. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. The Plant Journal, 2009, 57(5): 798-809.
doi: 10.1111/j.1365-313X.2008.03726.x pmid: 18980647
[35] LOURENÇO T, SAPETA H, FIGUEIREDO D D, RODRIGUES M, CORDEIRO A, ABREU I A, SAIBO N J, OLIVEIRA M M. Isolation and characterization of rice (Oryza sativa L.) E3-ubiquitin ligase OsHOS1 gene in the modulation of cold stress response. Plant Molecular Biology, 2013, 83(4/5): 351-363.
doi: 10.1007/s11103-013-0092-6
[36] SUN S K, XU X, TANG Z, TANG Z, HUANG X Y, WIRTZ M, HELL R, ZHAO F J. A molecular switch in sulfur metabolism to reduce arsenic and enrich selenium in rice grain. Nature Communications, 2021, 12: 1392.
doi: 10.1038/s41467-021-21282-5
[37] LIAO Y D, LIN K H, CHEN C C, CHIANG C M. Oryza sativa protein phosphatase 1a (OsPP1a) involved in salt stress tolerance in transgenic rice. Molecular Breeding, 2016, 36: 22.
doi: 10.1007/s11032-016-0446-2
[38] GIRI J, VIJ S, DANSANA P K, TYAGI A K. Rice A20/AN1 zinc- finger containing stress-associated proteins (SAP1/11) and a receptor- like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytologist, 2011, 191(3): 721-732.
doi: 10.1111/j.1469-8137.2011.03740.x
[39] MUKHOPADHYAY A, VIJ S, TYAGI A K.Overexpression of a zinc- finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proceedings of the National Academy of Sciences of the USA, 2004, 101(16): 6309-6314.
[40] ERRICHELLI L, DINI M S, LANEVE P, COLANTONI A, LEGNINI I, CAPAUTO D, ROSA A, DE SANTIS R, SCARFO R, PERUZZI G. FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons. Nature Communications, 2017, 8: 14741.
doi: 10.1038/ncomms14741 pmid: 28358055
[41] YIN J L, MA D F, LIU L C, XIA Y C, ZHU Y X. Biology features of circular RNAs and their research progress in plants. Acta Botanica Boreali-Occidentalia Sinica, 2017, 37(12): 2510-2518.
[42] LU T, CUI L, ZHOU Y, ZHU C, FAN D, GONG H, ZHAO Q, ZHOU C, ZHAO Y, LU D. Transcriptome-wide investigation of circular RNAs in rice. RNA, 2015, 21(12): 2076-2087
doi: 10.1261/rna.052282.115 pmid: 26464523
[43] HANSEN T B, JENSEN T I, CLAUSEN B H, BRAMSEN J B, FINSEN B, DAMGAARD C K. Natural RNA circles function as efficient microRNA sponges. Nature, 2013, 495: 384-388.
doi: 10.1038/nature11993
[44] MELONI D, OLIVA M, MARTINEZ C, CAMBRAIA J. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany, 2003, 49: 69-76.
doi: 10.1016/S0098-8472(02)00058-8
[45] GUTTERSON N, REUBER T L. Regulation of disease resistance pathways by AP2/ERF transcription factors. Current Opinion in Plant Biology, 2004, 7(4): 465-471.
pmid: 15231271
[46] NELSON D R. Plant cytochrome P450s from moss to poplar. Phytochemistry Reviews, 2006, 5(2/3): 193-204.
doi: 10.1007/s11101-006-9015-3
[47] SCHULZ P, HERDE M, ROMEIS T. Calcium-dependent protein kinases: Hubs in plant stress signaling and development. Plant Physiology, 2013, 163(2): 523-530.
doi: 10.1104/pp.113.222539 pmid: 24014579
[48] DAS R, PANDEY G. Expressional analysis and role of calcium regulated kinases in abiotic stress signaling. Current Genomics, 2010, 11(1): 2-13.
doi: 10.2174/138920210790217981 pmid: 20808518
[49] LI M Z, LI M F, LI D D, WANG S M, YIN H J. Overexpression of the Zygophyllum xanthoxylum aquaporin, ZxPIP1;3, promotes plant growth and stress tolerance. International Journal of Molecular Sciences, 2021, 22(4): 2112.
doi: 10.3390/ijms22042112
[50] CAO Y F, WU Y F, ZHENG Z, SONG F G. Overexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco. Physiological and Molecular Plant Pathology, 2006, 67(3/5): 202-211.
doi: 10.1016/j.pmpp.2006.01.004
[51] LIU C W, FUKUMOTO T, MATSUMOTO T, GENA P, FRASCARIA D, KANEKO T, KATSUHARA M, ZHONG S H, SUN X L, ZHU Y M, IWASAKI I, DING X D, CALAMITA G, KITAGAWA Y. Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiology and Biochemistry, 2013, 63: 151-158.
doi: 10.1016/j.plaphy.2012.11.018
[1] PENG HaiXia, KA DeYan, ZHANG TianXing, ZHOU MengDie, WU LinNan, XIN ZhuanXia, ZHAO HuiXian, MA Meng. Overexpression of Wheat TaCYP78A5 Increases Flower Organ Size [J]. Scientia Agricultura Sinica, 2023, 56(9): 1633-1645.
[2] WEI YongKang, YANG TianCong, ZANG ShaoLong, HE Li, DUAN JianZhao, XIE YingXin, WANG ChenYang, FENG Wei. Monitoring Wheat Lodging Based on UAV Multi-Spectral Image Feature Fusion [J]. Scientia Agricultura Sinica, 2023, 56(9): 1670-1685.
[3] HAN ZiXuan, FANG JingJing, WU XuePing, JIANG Yu, SONG XiaoJun, LIU XiaoTong. Synergistic Effects of Organic Carbon and Nitrogen Content in Water-Stable Aggregates as well as Microbial Biomass on Crop Yield Under Long-Term Straw Combined Chemical Fertilizers Application [J]. Scientia Agricultura Sinica, 2023, 56(8): 1503-1514.
[4] MA ShengLan, KUANG FuHong, LIN HongYu, CUI JunFang, TANG JiaLiang, ZHU Bo, PU QuanBo. Effects of Straw Incorporation Quantity on Soil Physical Characteristics of Winter Wheat-Summer Maize Rotation System in the Central Hilly Area of Sichuan Basin [J]. Scientia Agricultura Sinica, 2023, 56(7): 1344-1358.
[5] NAN Rui, YANG YuCun, SHI FangHui, ZHANG LiNing, MI TongXi, ZHANG LiQiang, LI ChunYan, SUN FengLi, XI YaJun, ZHANG Chao. Identification of Excellent Wheat Germplasms and Classification of Source-Sink Types [J]. Scientia Agricultura Sinica, 2023, 56(6): 1019-1034.
[6] CHANG ChunYi, CAO Yuan, GHULAM Mustafa, LIU HongYan, ZHANG Yu, TANG Liang, LIU Bing, ZHU Yan, YAO Xia, CAO WeiXing, LIU LeiLei. Effects of Powdery Mildew on Photosynthetic Characteristics and Quantitative Simulation of Disease Severity in Winter Wheat [J]. Scientia Agricultura Sinica, 2023, 56(6): 1061-1073.
[7] WANG XiaoXuan, ZHANG Min, ZHANG XinYao, WEI Peng, CHAI RuShan, ZHANG ChaoChun, ZHANG LiangLiang, LUO LaiChao, GAO HongJian. Effects of Different Varieties of Phosphate Fertilizer Application on Soil Phosphorus Transformation and Phosphorus Uptake and Utilization of Winter Wheat [J]. Scientia Agricultura Sinica, 2023, 56(6): 1113-1126.
[8] WANG Mai, DONG QingFeng, GAO ShenAo, LIU DeZheng, LU Shan, QIAO PengFang, CHEN Liang, HU YinGang. Genome-Wide Association Studies and Mining for Favorable Loci of Root Traits at Seedling Stage in Wheat [J]. Scientia Agricultura Sinica, 2023, 56(5): 801-820.
[9] FAN ZhiLong, HU FaLong, YIN Wen, FAN Hong, ZHAO Cai, YU AiZhong, CHAI Qiang. Response of Water Use Characteristics of Spring Wheat to Co- Incorporation of Green Manure and Wheat Straw in Arid Irrigation Region [J]. Scientia Agricultura Sinica, 2023, 56(5): 838-849.
[10] GUO Yan, JING YuHang, WANG LaiGang, HUANG JingYi, HE Jia, FENG Wei, ZHENG GuoQing. UAV Multispectral Image-Based Nitrogen Content Prediction and the Transferability Analysis of the Models in Winter Wheat Plant [J]. Scientia Agricultura Sinica, 2023, 56(5): 850-865.
[11] WANG JianFeng, CHENG JiaXin, SHU WeiXue, ZHANG YanRu, WANG XiaoJie, KANG ZhenSheng, TANG ChunLei. Functional Analysis of Effector Hasp83 in the Pathogenicity of Puccinia striiformis f. sp. tritici [J]. Scientia Agricultura Sinica, 2023, 56(5): 866-878.
[12] YAO YiJun, JU XingRong, WANG LiFeng. Lipid-Lowering Effects and Its Regulation Mechanism of Buckwheat Polyphenols in High-Fat Diet-Induced Obese Mice [J]. Scientia Agricultura Sinica, 2023, 56(5): 981-994.
[13] DING JinFeng, XU DongYi, DING YongGang, ZHU Min, LI ChunYan, ZHU XinKai, GUO WenShan. Effects of Cultivation Patterns on Grain Yield, Nitrogen Uptake and Utilization, and Population Quality of Wheat Under Rice-Wheat Rotation [J]. Scientia Agricultura Sinica, 2023, 56(4): 619-634.
[14] CHEN JiHao, ZHOU JieGuang, QU XiangRu, WANG SuRong, TANG HuaPing, JIANG Yun, TANG LiWei, $\boxed{\hbox{LAN XiuJin}}$, WEI YuMing, ZHOU JingZhong, MA Jian. Mapping and Analysis of QTL for Embryo Size-Related Traits in Tetraploid Wheat [J]. Scientia Agricultura Sinica, 2023, 56(2): 203-216.
[15] YAN YanGe, ZHANG ShuiQin, LI YanTing, ZHAO BingQiang, YUAN Liang. Effects of Dextran Modified Urea on Winter Wheat Yield and Fate of Nitrogen Fertilizer [J]. Scientia Agricultura Sinica, 2023, 56(2): 287-299.
Full text



No Suggested Reading articles found!