Scientia Agricultura Sinica ›› 2026, Vol. 59 ›› Issue (1): 90-100.doi: 10.3864/j.issn.0578-1752.2026.01.007

• PLANT PROTECTION • Previous Articles     Next Articles

The Photosystem II Protein NbPsbQ1 Inhibits Viral Infection by Promoting Photosynthetic Efficiency

FU Han(), YU Yang, AI Niu, ZHANG SiQing, YU LianWei, SUN ShuHao, ZHAO JinZhang, HAN XiaoYu, SHI Yan, YANG Xue*()   

  1. College of Plant Protection, Henan Agricultural University, Zhengzhou 450046
  • Received:2025-08-29 Accepted:2025-10-05 Online:2026-01-01 Published:2026-01-07
  • Contact: YANG Xue

Abstract:

【Background】Cucumber green mottle mosaic virus (CGMMV) is one of the important quarantined plant viruses in China. It mainly infects Cucurbitaceae crops, causing severe yield losses of Cucurbitaceae crops worldwide. The PsbQ protein (oxygen-evolving enhancer protein 3) is one of the proteins associated with the photosystem II (PSII) oxygen-evolving complex (OEC). It is involved in PSII assembly, stabilizes PSII function, and regulates plant responses to biotic and abiotic stresses. Previous studies have shown that CGMMV infection can significantly downregulate the expression of the host chloroplast regulatory gene NbPsbQ1. 【Objective】This study aims to clarify the mechanism by which NbPsbQ1 participates in CGMMV infection and provide a theoretical basis for the prevention and control of CGMMV infection. 【Method】The expression vector of NbPsbQ1-GFP and CGMMV CP was constructed, transformed into Agrobacterium GV3101 and infiltrated the tobacco leaves to observe the subcellular localization of NbPsbQ1 by confocal microscopy. qRT-PCR was used to analyze the transcriptional levels of NbPsbQ1 at different stages of CGMMV infection and after CP overexpression. The interaction between NbPsbQ1 and CP in vivo and in vitro was verified using bimolecular fluorescence complementation (BiFC), co-immunoprecipitation (Co-IP), and yeast two-hybrid (Y2H) assays, respectively. TRV-mediated gene silencing (VIGS) was employed to investigate the role of NbPsbQ1 during CGMMV infection. Transient overexpression of NbPsbQ1 was used to further verify the effect of NbPsbQ1 on the protein level and transcriptional level of CGMMV. The photosynthetic efficiency indicators of plants were determined after NbPsbQ1 silencing and at different stages of CGMMV infection, the effects of NbPsbQ1 and CGMMV on plant photosynthesis were analyzed. 【Result】Subcellular localization results showed that NbPsbQ1 was localized in chloroplasts, while CP was localized in the cytoplasm and nucleus. After CGMMV infection or CP overexpression, the transcriptional level of NbPsbQ1 was significantly downregulated compared with the control. Results from both BiFC and Co-IP assays demonstrated that NbPsbQ1 interacts with CP in vivo. Furthermore, this interaction causes the subcellular localization of NbPsbQ1 to shift from chloroplasts to the cytoplasm. However, the yeast two-hybrid (Y2H) assay confirmed that the two proteins do not interact in vitro. CGMMV was inoculated into TRV:NbPsbQ1 and TRV:00 plants. Partial systemic leaves of plants in both the TRV:NbPsbQ1 and TRV:00 plants began to show mottling and curling symptoms at 4 dpi. However, the number of symptomatic plants was consistently higher in the TRV:NbPsbQ1 plants than that in the control plants. Meanwhile, detection of mRNA and protein expression levels also indicated that silencing NbPsbQ1 effectively promoted CGMMV accumulation. Transient overexpression of NbPsbQ1 inhibited the accumulation of CP, further confirming that NbPsbQ1 suppresses CGMMV infection. Silencing of NbPsbQ1 significantly reduced the net photosynthetic rate (Pn), stomatal conductance (Gs), and transpiration rate (Tr) of plant leaves, while the intercellular CO2 concentration (Ci) increased significantly, indicating that NbPsbQ1 is involved in plant photosynthesis. Additionally, it was found that Gs and Tr decreased significantly, while Ci increased at 9 d during CGMMV infection. 【Conclusion】The CP of CGMMV interacts with NbPsbQ1 in vivo and alters its chloroplast localization. During the CGMMV infection, the expression level of NbPsbQ1 is downregulated, and photosynthetic efficiency is inhibited, thereby promoting the CGMMV accumulation in the late infection stage.

Key words: cucumber green mottle mosaic virus (CGMMV), NbPsbQ1, photosystem II (PSII), photosynthesis, pathogenic mechanism

Fig. 1

Subcellular localization of NbPsbQ1 (A) and CGMMV CP (B)"

Fig. 2

Effect of CGMMV infection and CP overexpression on the transcriptional level of NbPsbQ1"

Fig. 3

Verification of the interaction between NbPsbQ1 and CP"

Fig. 4

Effect of NbPsbQ1 silencing on CGMMV infection"

Fig. 5

Effect of transient overexpression of NbPsbQ1 on CGMMV accumulation"

Fig. 6

Effect of NbPsbQ1 silencing on photosynthetic parameters"

Fig. 7

Effect of CGMMV infection at different times on photosynthetic parameters of N. benthamiana"

[1]
DOMBROVSKY A, TRAN-NGUYEN L T T, JONES R A C. Cucumber green mottle mosaic virus: Rapidly increasing global distribution, etiology, epidemiology, and management. Annual Review of Phytopathology, 2017, 55: 231-256.

doi: 10.1146/annurev-phyto-080516-035349 pmid: 28590876
[2]
LING K S, LI R, ZHANG W. First report of cucumber green mottle mosaic virus infecting greenhouse cucumber in Canada. Plant Disease, 2014, 98(5): 701.
[3]
周红珍, 张志勇, 彭辉. 黄瓜绿斑驳花叶病毒病的发生症状及防控措施. 现代农业科技, 2013(18): 138, 140.
ZHOU H Z, ZHANG Z Y, PENG H. Occurrence symptoms and control measures of cucumber green mottle mosaic virus disease. Modern Agricultural Science and Technology, 2013(18): 138, 140. (in Chinese)
[4]
林燚, 杨瑜斌, 王驰, 王文华, 毛玲荣. 温台地区西瓜发生黄瓜绿斑驳花叶病毒病调查初报. 浙江农业科学, 2012(1): 83-85.
LIN Y, YANG Y B, WANG C, WANG W H, MAO L R. Preliminary report on the occurrence of cucumber green mottle mosaic virus disease on watermelon in Wentai region. Journal of Zhejiang Agricultural Sciences, 2012(1): 83-85. (in Chinese)
[5]
UGAKI M, TOMIYAMA M, KAKUTANI T, HIDAKA S, KIGUCHI T, NAGATA R, SATO T, MOTOYOSHI F, NISHIGUCHI M. The complete nucleotide sequence of cucumber green mottle mosaic virus (SH strain) genomic RNA. Journal of General Virology, 1991, 72(7): 1487-1495.

doi: 10.1099/0022-1317-72-7-1487
[6]
YOO Y H, HONG W J, JUNG K H. A systematic view exploring the role of chloroplasts in plant abiotic stress responses. BioMed Research International, 2019, 2019: 6534745.
[7]
NOMURA H, KOMORI T, UEMURA S, KANDA Y, SHIMOTANI K, NAKAI K, FURUICHI T, TAKEBAYASHI K, SUGIMOTO T, SANO S, SUWASTIKA I N, FUKUSAKI E, YOSHIOKA H, NAKAHIRA Y, SHIINA T. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nature Communications, 2012, 3: 926.

doi: 10.1038/ncomms1926
[8]
SERRANO I, AUDRAN C, RIVAS S. Chloroplasts at work during plant innate immunity. Journal of Experimental Botany, 2016, 67(13): 3845-3854.

doi: 10.1093/jxb/erw088 pmid: 26994477
[9]
SOWDEN R G, WATSON S J, JARVIS P. The role of chloroplasts in plant pathology. Essays in Biochemistry, 2018, 62(1): 21-39.

doi: 10.1042/EBC20170020 pmid: 29273582
[10]
DE TORRES ZABALA M, LITTLEJOHN G, JAYARAMAN S, STUDHOLME D, BAILEY T, LAWSON T, TILLICH M, LICHT D, BÖLTER B, DELFINO L, TRUMAN W, MANSFIELD J, SMIRNOFF N, GRANT M. Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nature Plants, 2015, 1: 15074.

doi: 10.1038/nplants.2015.74 pmid: 27250009
[11]
WANG X T, JIANG Z H, YUE N, JIN X J, ZHANG X, LI Z L, ZHANG Y L, WANG X B, HAN C G, YU J L, LI D W. Barley stripe mosaic virus γb protein disrupts chloroplast antioxidant defenses to optimize viral replication. The EMBO Journal, 2021, 40(16): e107660.

doi: 10.15252/embj.2021107660
[12]
BHATTACHARYYA D, CHAKRABORTY S. Chloroplast: The Trojan horse in plant-virus interaction. Molecular Plant Pathology, 2018, 19(2): 504-518.

doi: 10.1111/mpp.12533 pmid: 28056496
[13]
MEDINA-PUCHE L, TAN H, DOGRA V, WU M S, ROSAS-DIAZ T, WANG L P, DING X, ZHANG D, FU X, KIM C, LOZANO-DURAN R. A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell, 2020, 182(5): 1109-1124.

doi: 10.1016/j.cell.2020.07.020
[14]
SIROHIWAL A, PANTAZIS D A. Functional water networks in fully hydrated photosystem II. Journal of the American Chemical Society, 2022, 144(48): 22035-22050.

doi: 10.1021/jacs.2c09121
[15]
BARTHEL S, BERNÁT G, SEIDEL T, RUPPRECHT E, KAHMANN U, SCHNEIDER D. Thylakoid membrane maturation and PSII activation are linked in greening Synechocystis sp. PCC 6803 cells. Plant Physiology, 2013, 163(2): 1037-1046.

doi: 10.1104/pp.113.224428
[16]
KONG L F, WU J X, LU L N, XU Y, ZHOU X P. Interaction between rice stripe virus disease-specific protein and host PsbP enhances virus symptoms. Molecular Plant, 2014, 7(4): 691-708.

doi: 10.1093/mp/sst158 pmid: 24214893
[17]
ABBINK T E, PEART J R, MOS T N, BAULCOMBE D C, BOL J F, LINTHORST H J. Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. Virology, 2002, 295(2): 307-319.

doi: 10.1006/viro.2002.1332 pmid: 12033790
[18]
GENG C, YAN Z Y, CHENG D J, LIU J, TIAN Y P, ZHU C X, WANG H Y, LI X D. Tobacco vein banding mosaic virus 6K2 protein hijacks NbPsbO1 for virus replication. Scientific Reports, 2017, 7: 43455.

doi: 10.1038/srep43455 pmid: 28230184
[19]
BALASUBRAMANIAM M, KIM B S, HUTCHENS-WILLIAMS H M, LOESCH-FRIES L S. The photosystem II oxygen-evolving complex protein PsbP interacts with the coat protein of alfalfa mosaic virus and inhibits virus replication. Molecular Plant-Microbe Interactions, 2014, 27(10): 1107-1118.

doi: 10.1094/MPMI-02-14-0035-R pmid: 24940990
[20]
HORNÍČÁKOVÁ M, KOHOUTOVÁ J, SCHLAGNITWEIT J, WOHLSCHLAGER C, ETTRICH R, FIALA R, SCHOEFBERGER W, MÜLLER N. Backbone assignment and secondary structure of the PsbQ protein from photosystem II. Biomolecular NMR Assignments, 2011, 5(2): 169-175.

doi: 10.1007/s12104-011-9293-6 pmid: 21259076
[21]
ALLAHVERDIYEVA Y, SUORSA M, ROSSI F, PAVESI A, KATER M M, ANTONACCI A, TADINI L, PRIBIL M, SCHNEIDER A, WANNER G, LEISTER D, ARO E M, BARBATO R, PESARESI P. Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen- evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms. The Plant Journal, 2013, 75(4): 671-684.

doi: 10.1111/tpj.2013.75.issue-4
[22]
MARTIN W F, CERFF R. Physiology, phylogeny, early evolution, and GAPDH. Protoplasma, 2017, 254(5): 1823-1834.

doi: 10.1007/s00709-017-1095-y pmid: 28265765
[23]
PÉREZ-BUENO M L, BARÓN M, GARCÍA-LUQUE I. PsbO, PsbP, and PsbQ of photosystem II are encoded by gene families in Nicotiana benthamiana. . Structure and functionality of their isoforms. Photosynthetica, 2011, 49(4): 573-580.
[24]
ZHOU F H, FENG X, JIANG A L, ZHU P F. Mutations in the BoPQL2 gene enhance the sensitivity to low temperature and affect the leaf margin coloration in ornamental kale. Scientia Horticulturae, 2024, 323: 112540.

doi: 10.1016/j.scienta.2023.112540
[25]
ZAGORŠCAK M, ABDELHAKIM L, RODRIGUEZ-GRANADOS N Y, ŠIROKÁ J, GHATAK A, BLEKER C, BLEJEC A, ZRIMEC J, NOVÁK O, PĚNČÍK A, et al. Integration of multi-omics data and deep phenotyping provides insights into responses to single and combined abiotic stress in potato. Plant Physiology, 2025, 197(4): kiaf126.
[26]
BERTAMINI M, MUTHUCHELIAN K, RUBINIGG M, ZORER R, NEDUNCHEZHIAN N. Low-night temperature (LNT) induced changes of photosynthesis in grapevine (Vitis vinifera L.) plants. Plant Physiology and Biochemistry, 2005, 43(7): 693-699.

doi: 10.1016/j.plaphy.2005.06.001
[27]
姜兴林, 于连伟, 付涵, 艾妞, 崔荧钧, 李好海, 夏子豪, 袁虹霞, 李洪连, 杨雪, 施艳. 转录因子NbMYB1R1通过促进活性氧积累抑制病毒侵染. 中国农业科学, 2024, 57(8): 1490-1505. doi: 10.3864/j.issn.0578-1752.2024.08.006.
JIANG X L, YU L W, FU H, AI N, CUI Y J, LI H H, XIA Z H, YUAN H X, LI H L, YANG X, SHI Y. The transcription factor NbMYB1R1 inhibits viral infection by promoting ROS accumulation. Scientia Agricultura Sinica, 2024, 57(8): 1490-1505. doi: 10.3864/j.issn.0578-1752.2024.08.006. (in Chinese)
[28]
RODRÍGUEZ-HERVA J J, GONZÁLEZ-MELENDI P, CUARTAS- LANZA R, ANTÚNEZ-LAMAS M, RÍO-ÁLVAREZ I, LI Z, LÓPEZ-TORREJÓN G, DÍAZ I, DEL POZO J C, CHAKRAVARTHY S, COLLMER A, RODRÍGUEZ-PALENZUELA P, LÓPEZ-SOLANILLA E. A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses. Cellular Microbiology, 2012, 14(5): 669-681.

doi: 10.1111/cmi.2012.14.issue-5
[29]
HUANG C P, PENG J B, ZHANG W, CHETHANA T, WANG X C, WANG H, YAN J Y. LtGAPR1 is a novel secreted effector from Lasiodiplodia theobromae that interacts with NbPsQ2 to negatively regulate infection. Journal of Fungi, 2023, 9(2): 188.

doi: 10.3390/jof9020188
[30]
ZHAI Y S, YUAN Q, QIU S S, LI M M, ZHENG H Y, WU G W, LU Y W, PENG J J, RAO S F, CHEN J P, YAN F. Turnip mosaic virus impairs perinuclear chloroplast clustering to facilitate viral infection. Plant, Cell and Environment, 2021, 44(11): 3681-3699.

doi: 10.1111/pce.v44.11
[31]
LI Z D, LI C Y, FU S, LIU Y, XU Y, WU J X, WANG Y Q, ZHOU X P. NSvc4 encoded by rice stripe virus targets host chloroplasts to suppress chloroplast-mediated defense. Viruses, 2022, 14(1): 36.

doi: 10.3390/v14010036
[32]
PFANNSCHMIDT T. Chloroplast redox signals: How photosynthesis controls its own genes. Trends in Plant Science, 2003, 8(1): 33-41.

doi: 10.1016/s1360-1385(02)00005-5 pmid: 12523998
[33]
HUANG T Z, ZHANG X S, WANG Q C, GUO Y R, XIE H, LI L, ZHANG P, LIU J N, QIN P. Metabolome and transcriptome profiles in quinoa seedlings in response to potassium supply. BMC Plant Biology, 2022, 22(1): 604.

doi: 10.1186/s12870-022-03928-8 pmid: 36539684
[34]
于力, 郭世荣, 朱为民, 阎君, 黑银秀. 番茄黄化曲叶病毒对番茄叶片光合特性和叶绿体超微结构的影响. 西北植物学报, 2011, 31(7): 1355-1359.
YU L, GUO S R, ZHU W M, YAN J, HEI Y X. Effects of tomato yellow leaf curl virus on photosynthetic characteristics and chloroplast ultra-structure of the tomato leaves. Acta Botanica Boreali-Occidentalia Sinica, 2011, 31(7): 1355-1359. (in Chinese)
[35]
易龙, 陈毅群, 李双花, 黄爱军. 柑橘衰退病毒侵染对‘赣南早’脐橙植株组织结构及光合作用的影响. 果树学报, 2020, 37(4): 574-581.
YI L, CHEN Y Q, LI S H, HUANG A J. Structural and photosynthetic changes in ‘Gannanzao’ navel orange plants infected with citrus tristeza virus. Journal of Fruit Science, 2020, 37(4): 574-581. (in Chinese)
[1] ZHANG Han, ZHANG YuQi, LI JingLai, XU Hong, LI WeiHuan, LI Tao. Effects of LED Supplementary Lighting on Production and Leaf Physiological Properties of Substrate-Cultivated Strawberry in Chinese Solar Greenhouse [J]. Scientia Agricultura Sinica, 2025, 58(5): 975-990.
[2] QIU HaiLong, LI Pan, ZHANG DianKai, FAN ZhiLong, HU FaLong, CHEN GuiPing, FAN Hong, HE Wei, YIN Wen, ZHAO LianHao. Compensatory Effects of Multiple Cropping Green Manure on Growth and Yield Loss of Nitrogen-Reduced Spring Wheat in Oasis Irrigation Areas of Northwest China [J]. Scientia Agricultura Sinica, 2025, 58(3): 443-459.
[3] ZHANG XiangKun, LI JiaYing, QIAO RuMeng, HE JingLei, WANG Li, SHI XiaoXin, DU GuoQiang. Effects of GFabV Under Different Zn Levels on Photosynthetic Efficiency and Photosynthesis-Related Gene Expression of ‘Shine Muscat’ Grapevine [J]. Scientia Agricultura Sinica, 2025, 58(24): 5190-5200.
[4] XU QiuYun, ZHOU WeiDi, HAN ChengLong, GU YanJie. Effects of Different Phosphorus Fertilizer Application Rates on Photosynthetic Characteristics, Yield and Water Use Efficiency of Broad Bean Mulched in Alpine Region [J]. Scientia Agricultura Sinica, 2025, 58(10): 1917-1933.
[5] JIANG XingLin, YU LianWei, FU Han, AI Niu, CUI YingJun, LI HaoHai, XIA ZiHao, YUAN HongXia, LI HongLian, YANG Xue, SHI Yan. The Transcription Factor NbMYB1R1 Inhibits Viral Infection by Promoting ROS Accumulation [J]. Scientia Agricultura Sinica, 2024, 57(8): 1490-1505.
[6] PEI ShuYao, CAO HongXia, ZHANG ZeYu, ZHAO FangYang, LI ZhiJun. Physiological Response of Potted Tomatoes to NaCl and Na2SO4 Brackish Water Irrigation [J]. Scientia Agricultura Sinica, 2024, 57(3): 570-583.
[7] XIN Lang, SONG JiaWen, FU YuanYuan, TANG MaoSong, JING LingKun, WANG XingPeng. Effects of Saline-Fresh Water Rotation Irrigation on Photosynthetic Characteristics and Leaf Ultrastructure of Tomato Plants in Greenhouse [J]. Scientia Agricultura Sinica, 2024, 57(19): 3784-3798.
[8] HE Yong, FAN XiaoZhu, CHEN XinYue, DUAN ShuJing, HU TingTing, XIE RuXue, WANG YuQing, CHEN Jing. Screening and Verification of Pepper Host Factors Interacting with the 126 kDa Protein of Pepper Mild Mottle Virus by Yeast Two-Hybrid System [J]. Scientia Agricultura Sinica, 2024, 57(15): 2986-2996.
[9] HE Jiang, DING Ying, LOU XiangDi, JI DongLing, ZHANG XiangXiang, WANG YongHui, ZHANG WeiYang, WANG ZhiQin, WANG WeiLu, YANG JianChang. Difference in the Comprehensive Response of Dry Matter Accumulation of Rice at Tillering Stage to Rising Atmospheric CO2 Concentration and Nitrogen Nutrition and Its Physiological Mechanism [J]. Scientia Agricultura Sinica, 2023, 56(6): 1045-1060.
[10] YANG Sha, LIU KeKe, LIU Ying, GUO Feng, WANG JianGuo, GAO HuaXin, MENG JingJing, ZHANG JiaLei, WAN ShuBo. The Molecular Mechanism of Pod Yield Difference Between Single- Seeding Precision Sowing and Multi-Seeds Sowing of Peanut Based on Transcriptome Analysis [J]. Scientia Agricultura Sinica, 2023, 56(22): 4386-4402.
[11] TENG YunFei, SHANG Bin, TAO XiuPing. Nutritional Effects of Liquid Digestate on Tomatoes Grown in Facility Substrates [J]. Scientia Agricultura Sinica, 2023, 56(19): 3869-3878.
[12] YU LianWei, JIANG XingLin, YANG LingLing, WANG He, ZHANG YuYang, XIE LiNa, XIA ZiHao, LI HongLian, YANG Xue, SHI Yan. Function of Transcription Factor NbERF RAP2-1 in Cucumber Green Mottle Mosaic Virus Infection [J]. Scientia Agricultura Sinica, 2023, 56(15): 2919-2928.
[13] CHU YanMeng, MAO YingChao, CAI Jian, ZHOU Qin, DAI TingBo, WANG Xiao, JIANG Dong. Effect of Phytochlorin Iron on Stress Tolerance to Waterlogging in Wheat [J]. Scientia Agricultura Sinica, 2023, 56(10): 1848-1858.
[14] LI YiLing, PENG XiHong, CHEN Ping, DU Qing, REN JunBo, YANG XueLi, LEI Lu, YONG TaiWen, YANG WenYu. Effects of Reducing Nitrogen Application on Leaf Stay-Green, Photosynthetic Characteristics and System Yield in Maize-Soybean Relay Strip Intercropping [J]. Scientia Agricultura Sinica, 2022, 55(9): 1749-1762.
[15] CHEN TingTing, FU WeiMeng, YU Jing, FENG BaoHua, LI GuangYan, FU GuanFu, TAO LongXing. The Photosynthesis Characteristics of Colored Rice Leaves and Its Relation with Antioxidant Capacity and Anthocyanin Content [J]. Scientia Agricultura Sinica, 2022, 55(3): 467-478.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!