SPL50 Regulates Cell Death and Resistance to Magnaporthe Oryzae in Rice.
SPL50
ARM repeat protein
Cell death
Disease resistance
Rice
Journal
Rice (New York, N.Y.)
ISSN: 1939-8425
Titre abrégé: Rice (N Y)
Pays: United States
ID NLM: 101503136
Informations de publication
Date de publication:
13 Aug 2024
13 Aug 2024
Historique:
received:
26
04
2024
accepted:
08
08
2024
medline:
13
8
2024
pubmed:
13
8
2024
entrez:
13
8
2024
Statut:
epublish
Résumé
The identification of spotted leaf 50 (spl50), a novel lesion mimic mutant (LMM) in rice, provides critical insights into the mechanisms underlying programmed cell death (PCD) and innate immunity in plants. Based on ethyl methane sulfonate (EMS)-induced mutagenesis, the spl50 mutant mimics hypersensitive responses in the absence of pathogen by displaying spontaneous necrotic lesions after the tillering phase. SPL50, an ARM repeat protein essential for controlling reactive oxygen species (ROS) metabolism and boosting resistance to blast disease, was identified by map-based cloning techniques. This work also demonstrates the detrimental effects of spl50 on photosynthetic efficiency and chloroplast development. The crucial significance of SPL50 in cellular signaling and stress response is shown by its localization to the cytoplasm and constitutive expression in various plant tissues. In light of growing concerns regarding global food security, this study highlights the pivotal role of SPL50 in regulating programmed cell death (PCD) and enhancing the immune response in plants, contributing to strategies for improving crop disease resistance. The novel identification of the SPL50 gene in rice, encoding an ARM repeat protein, reveals its pivotal role in regulating PCD and innate immune responses independently of pathogen attack.
Sections du résumé
BACKGROUND
BACKGROUND
The identification of spotted leaf 50 (spl50), a novel lesion mimic mutant (LMM) in rice, provides critical insights into the mechanisms underlying programmed cell death (PCD) and innate immunity in plants.
RESULTS
RESULTS
Based on ethyl methane sulfonate (EMS)-induced mutagenesis, the spl50 mutant mimics hypersensitive responses in the absence of pathogen by displaying spontaneous necrotic lesions after the tillering phase. SPL50, an ARM repeat protein essential for controlling reactive oxygen species (ROS) metabolism and boosting resistance to blast disease, was identified by map-based cloning techniques. This work also demonstrates the detrimental effects of spl50 on photosynthetic efficiency and chloroplast development. The crucial significance of SPL50 in cellular signaling and stress response is shown by its localization to the cytoplasm and constitutive expression in various plant tissues. In light of growing concerns regarding global food security, this study highlights the pivotal role of SPL50 in regulating programmed cell death (PCD) and enhancing the immune response in plants, contributing to strategies for improving crop disease resistance.
CONCLUSIONS
CONCLUSIONS
The novel identification of the SPL50 gene in rice, encoding an ARM repeat protein, reveals its pivotal role in regulating PCD and innate immune responses independently of pathogen attack.
Identifiants
pubmed: 39136883
doi: 10.1186/s12284-024-00731-x
pii: 10.1186/s12284-024-00731-x
doi:
Types de publication
Journal Article
Langues
eng
Pagination
51Subventions
Organisme : the Natural Science Foundation of Zhejiang
ID : LY23C130001
Organisme : the National Natural Science Foundation of China
ID : 32370328
Organisme : Ten-thousand Talents Plan of Zhejiang Province
ID : 2022R52027
Organisme : the Science and Technology Project of Hangzhou
ID : 202203B03
Informations de copyright
© 2024. The Author(s).
Références
Byun MY, Cui LH, Oh TK, Jung YJ, Lee A, Park KY, Kang BG, Kim WT (2017) Homologous U-box E3 ubiquitin ligases OsPUB2 and OsPUB3 are involved in the positive regulation of low temperature stress response in Rice (Oryza sativa L). Front Plant Sci 8:16
pubmed: 28163713
pmcid: 5247461
doi: 10.3389/fpls.2017.00016
Cai L, Yan M, Yun H, Tan J, Du D, Sun H, Guo Y, Sang X, Zhang C (2021) Identification and fine mapping of lesion mimic mutant spl36 in rice (Oryza sativa L). Breed Sci 71(5):510–519
pubmed: 35087315
pmcid: 8784353
doi: 10.1270/jsbbs.20160
Chen X, Hao L, Pan J, Zheng X, Jiang G, Jin Y, Gu Z, Qian Q, Zhai W, Ma BJMB (2012) SPL5, a cell death and defense-related gene, encodes a putative splicing factor 3b subunit 3 (SF3b3) in rice. Mol Breed 30(2):939–949
doi: 10.1007/s11032-011-9677-4
Chen E, Hou Q, Liu K, Gu Z, Dai B, Wang A, Feng Q, Zhao Y, Zhou C, Zhu J, Shangguan Y, Wang Y, Lv D, Fan D, Huang T, Wang Z, Huang X, Han B (2023) Armadillo repeat only protein GS10 negatively regulates brassinosteroid signaling to control rice grain size. Plant Physio 192(2):967–981
doi: 10.1093/plphys/kiad117
Cui Y, Peng Y, Zhang Q, Xia S, Ruan B, Xu Q, Yu X, Zhou T, Liu H, Zeng D, Zhang G, Gao Z, Hu J, Zhu L, Shen L, Guo L, Qian Q, Ren D (2021) Disruption of EARLY LESION LEAF 1, encoding a cytochrome P450 monooxygenase, induces ROS accumulation and cell death in rice. Plant J 105(4):942–956
pubmed: 33190327
doi: 10.1111/tpj.15079
Du D, Zhang C, Xing Y, Lu X, Cai L, Yun H, Zhang Q, Zhang Y, Chen X, Liu M, Sang X, Ling Y, Yang Z, Li Y, Lefebvre B, He G (2021) The CC-NB-LRR OsRLR1 mediates rice disease resistance through interaction with OsWRKY19. Plant Biotechnol J 19(5):1052–1064
pubmed: 33368943
pmcid: 8131040
doi: 10.1111/pbi.13530
Huang L, Sun Q, Qin F, Li C, Zhao Y, Zhou DX (2007) Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol 144(3):1508–1519
pubmed: 17468215
pmcid: 1914135
doi: 10.1104/pp.107.099473
Kulich I, Vogler F, Bleckmann A, Cyprys P, Lindemeier M, Fuchs I, Krassini L, Schubert T, Steinbrenner J, Beynon J, Falter-Braun P, Längst G, Dresselhaus T, Sprunck S (2020) ARMADILLO REPEAT ONLY proteins confine rho GTPase signalling to polar growth sites. Nat Plants 6(10):1275–1288
pubmed: 33020609
doi: 10.1038/s41477-020-00781-1
Kurien BT, Scofield RH (2006) Western blotting. Methods 38(4):283–293
pubmed: 16483794
doi: 10.1016/j.ymeth.2005.11.007
Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8(6):263–271
pubmed: 12818660
doi: 10.1016/S1360-1385(03)00108-0
Lv Q, Li X, Jin X, Sun Y, Wu Y, Wang W, Huang J (2022) Rice OsPUB16 modulates the ‘SAPK9-OsMADS23-OsAOC’ pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. PLoS Genet 18(11):e1010520
pubmed: 36441771
pmcid: 9731423
doi: 10.1371/journal.pgen.1010520
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410
pubmed: 12234732
doi: 10.1016/S1360-1385(02)02312-9
Mu X, Li J, Dai Z, Xu L, Fan T, Jing T, Chen M, Gou M (2021) Commonly and specifically activated defense responses in Maize Disease Lesion mimic mutants revealed by Integrated Transcriptomics and Metabolomics Analysis. Front Plant Sci 12:638792
pubmed: 34079566
pmcid: 8165315
doi: 10.3389/fpls.2021.638792
Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76(5):789–791
pubmed: 7907279
doi: 10.1016/0092-8674(94)90353-0
Rao Y, Jiao R, Wang S, Wu X, Ye H, Pan C, Li S, Xin D, Zhou W, Dai G, Hu J, Ren D, Wang Y (2021) SPL36 encodes a receptor-like protein kinase that regulates programmed cell death and defense responses in Rice. Rice 14(1):34
doi: 10.1186/s12284-021-00475-y
Ren D, Hu J, Xu Q, Cui Y, Zhang Y, Zhou T, Rao Y, Xue D, Zeng D, Zhang G, Gao Z, Zhu L, Shen L, Chen G, Guo L, Qian Q (2018) FZP determines grain size and sterile lemma fate in rice. J Exp Bot 69(20):4853–4866
pubmed: 30032251
pmcid: 6137974
doi: 10.1093/jxb/ery264
Ruan B, Hua Z, Zhao J, Zhang B, Ren D, Liu C, Yang S, Zhang A, Jiang H, Yu H, Hu J, Zhu L, Chen G, Shen L, Dong G, Zhang G, Zeng D, Guo L, Qian Q, Gao Z (2019) OsACL-A2 negatively regulates cell death and disease resistance in rice. Plant Biotechnol J 17(7):1344–1356
pubmed: 30582769
pmcid: 6576086
doi: 10.1111/pbi.13058
Rubio V, Shen Y, Saijo Y, Liu Y, Gusmaroli G, Dinesh-Kumar SP, Deng XW (2005) An alternative tandem affinity purification strategy applied to Arabidopsis protein complex isolation. Plant J 41(5):767–778
pubmed: 15703063
doi: 10.1111/j.1365-313X.2004.02328.x
Simeonova E, Sikora A, Charzyńska M, Mostowska AJP (2000) Aspects of programmed cell death during leaf senescence of mono and dicotyledonous plants. Protoplasma 214(1–2):93–101
doi: 10.1007/BF02524266
Sun J, Zhang M, Qi X, Doyle C, Zheng H (2020) Armadillo-repeat kinesin1 interacts with Arabidopsis atlastin RHD3 to move ER with plus-end of microtubules. Nat Commun 11(1):5510
pubmed: 33139737
pmcid: 7606470
doi: 10.1038/s41467-020-19343-2
Sun J, Song W, Chang Y, Wang Y, Lu T, Zhang Z (2021) OsLMP1, encoding a deubiquitinase, regulates the Immune response in Rice. Front Plant Sci 12:814465
pubmed: 35116051
doi: 10.3389/fpls.2021.814465
Takahashi A, Kawasaki T, Henmi K, Shi IK, Kodama O, Satoh H, Shimamoto K (1999) Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J 17(5):535–545
pubmed: 10205906
doi: 10.1046/j.1365-313X.1999.00405.x
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47(6):969–976
pubmed: 16961734
doi: 10.1111/j.1365-313X.2006.02836.x
Wang L, Ma H, Fu L, Yao J (2014) Kpna7 interacts with egg-specific nuclear factors in the rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev 81(12):1136–1145
pubmed: 25511304
doi: 10.1002/mrd.22433
Wang J, Qu B, Dou S, Li L, Yin D, Pang Z, Zhou Z, Tian M, Liu G, Xie Q, Tang D, Chen X, Zhu L (2015) The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol 15:49
pubmed: 25849162
pmcid: 4330927
doi: 10.1186/s12870-015-0442-4
Wang S, Lei C, Wang J, Ma J, Tang S, Wang C, Zhao K, Tian P, Zhang H, Qi C, Cheng Z, Zhang X, Guo X, Liu L, Wu C, Wan J (2017) SPL33, encoding an eEF1A-like protein, negatively regulates cell death and defense responses in rice. J Exp Bot 68(5):899–913
pubmed: 28199670
pmcid: 5441852
doi: 10.1093/jxb/erx001
Wang K, Li S, Chen L, Tian H, Chen C, Fu Y, Du H, Hu Z, Li R, Du Y, Li J, Zhao Q, Du C (2023a) E3 ubiquitin ligase OsPIE3 destabilises the B-lectin receptor-like kinase PID2 to control blast disease resistance in rice. New Phytol 237(5):1826–1842
pubmed: 36440499
doi: 10.1111/nph.18637
Wang Y, Abrouk M, Gourdoupis S, Koo DH, Karafiátová M, Molnár I, Holušová K, Doležel J, Athiyannan N, Cavalet-Giorsa E, Jaremko Ł, Poland J, Krattinger SG (2023b) An unusual tandem kinase fusion protein confers leaf rust resistance in wheat. Nat Genet 55(6):914–920
pubmed: 37217716
pmcid: 10260399
doi: 10.1038/s41588-023-01401-2
Wolter M, Hollricher K, Salamini F, Schulze-Lefert P (1993) The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol Gen Genet 239(1–2):122–128
pubmed: 8510641
doi: 10.1007/BF00281610
Xu X, Wang H, Liu J, Han S, Lin M, Guo Z, Chen X (2022) OsWRKY62 and OsWRKY76 interact with importin α1s for negative regulation of defensive responses in Rice Nucleus. Rice 15(1):12
pubmed: 35184252
pmcid: 8859016
doi: 10.1186/s12284-022-00558-4
Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci U S A 99(11):7530–7535
pubmed: 12032317
pmcid: 124274
doi: 10.1073/pnas.112209199
Yoshida MW, Hakozaki M, Goshima G (2023) Armadillo repeat-containing kinesin represents the versatile plus-end-directed transporter in Physcomitrella. Nat Plants 9(5):733–748
pubmed: 37142749
doi: 10.1038/s41477-023-01397-x
Yu G, Matny O, Gourdoupis S, Rayapuram N, Aljedaani FR, Wang YL, Nürnberger T, Johnson R, Crean EE, Saur IM, Gardener C, Yue Y, Kangara N, Steuernagel B, Hayta S, Smedley M, Harwood W, Patpour M, Wu S, Poland J, Jones JDG, Reuber TL, Ronen M, Sharon A, Rouse MN, Xu S, Holušová K, Bartoš J, Molnár I, Karafiátová M, Hirt H, Blilou I, Jaremko Ł, Doležel J, Steffenson BJ, Wulff BBH (2023) The wheat stem rust resistance gene Sr43 encodes an unusual protein kinase. Nat Genet 55(6):921–926
pubmed: 37217714
pmcid: 10260397
doi: 10.1038/s41588-023-01402-1
Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004) Spotted leaf 11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16(10):2795–2808
pubmed: 15377756
pmcid: 520972
doi: 10.1105/tpc.104.025171
Zhang P, Ma X, Liu L, Mao C, Hu Y, Yan B, Guo J, Liu X, Shi J, Lee GS, Pan X, Deng Y, Zhang Z, Kang Z, Qiao Y (2023) MEDIATOR SUBUNIT 16 negatively regulates rice immunity by modulating PATHOGENESIS RELATED 3 activity. Plant Physiol 192(2):1132–1150
pubmed: 36815292
pmcid: 10231465
doi: 10.1093/plphys/kiad120
Zhang H, Yang J, Liu M, Xu X, Yang L, Liu X, Peng Y, Zhang Z (2024) Early molecular events in the interaction between Magnaporthe oryzae and rice. Phytopathol Res 6(1):9
doi: 10.1186/s42483-024-00226-z
Zhao H, Wang X, Jia Y, Minkenberg B, Wheatley M, Fan J, Jia MH, Famoso A, Edwards JD, Wamishe Y, Valent B, Wang GL, Yang Y (2018) The rice blast resistance gene ptr encodes an atypical protein required for broad-spectrum disease resistance. Nat Commun 9(1):2039
pubmed: 29795191
pmcid: 5966436
doi: 10.1038/s41467-018-04369-4
Zhao J, Liu X, Wang M, Xie L, Wu Z, Yu J, Wang Y, Zhang Z, Jia Y, Liu Q (2022) The miR528-D3 module regulates plant height in rice by modulating the gibberellin and abscisic acid metabolisms. Rice 15:27
pubmed: 35596029
pmcid: 9123139
doi: 10.1186/s12284-022-00575-3
Zhao J, Meng X, Zhang Z, Wang M, Nie F, Liu Q (2023) OsLPR5 encoding ferroxidase positively regulates the tolerance to salt stress in rice. Int J Mol Sci 24(9):8115
pubmed: 37175822
pmcid: 10179522
doi: 10.3390/ijms24098115
Zhu X, Ze M, Chern M, Chen X, Wang J (2020) Deciphering rice lesion mimic mutants to understand molecular network governing plant immunity and growth. Rice Sci 27(4):278–288
doi: 10.1016/j.rsci.2020.05.004
Zou T, Li G, Liu M, Liu R, Yang S, Wang K, Lu L, Ye Q, Liu J, Liang J, Deng Q, Wang S, Zhu J, Liang Y, Liu H, Yu X, Sun C, Li P, Li S (2023) A ubiquitin-specific protease functions in regulating cell death and immune responses in rice. Plant Cell Environ 46(4):1312–1326
pubmed: 36624579
doi: 10.1111/pce.14540