Rice Science ›› 2024, Vol. 31 ›› Issue (3): 285-299.DOI: 10.1016/j.rsci.2023.12.003
• Reviews • Previous Articles Next Articles
Hou Xinyue1,2, Wang Yuping2, Qian Qian1(
), Ren Deyong1()
Received:2023-10-15
Accepted:2023-12-07
Online:2024-05-28
Published:2024-06-04
Contact:
Qian Qian, Ren Deyong
Hou Xinyue, Wang Yuping, Qian Qian, Ren Deyong. Molecular Mechanism of Rice Necrotic Lesion for Optimized Yield and Disease Resistance[J]. Rice Science, 2024, 31(3): 285-299.
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Fig. 1. Causes of rice necrotic lesion formation. Alterations in the expression of related genes, ROS enzyme system, PCD, membrane proteins, chloroplast structure, chloroplast synthesis, and environmental factors (light and humidity) lead to cell death, ROS accumulation, thereby producing necrotic lesions. ROS, Reactive oxygen species; PCD, Programmed cell death; JA, Jasmonic acid; SA, Salicylic acid; ET, Ethylene; CAT, Catalase; SOD, Superoxide dismutase; APX, Ascorbate peroxidase; PRs, Pathogenesis-related genes. ‘→’ symbol indicates activation or next step, and ‘├’ symbol indicates inhibition.
Fig. 2. Necrotic lesion genes are involved in mitogen-activated protein kinase (MAPK) signaling and ubiquitine pathways. Plants regulate in vivo defense responses by adjusting EDS1 phosphorylation and MPKK10.2 cascade status. SPL11-SDS2, SPL11-SPIN6, and RAC1 can jointly participate in pathogen resistance signaling pathways. SPL11 is a negative regulator of plant cell death and defense, and plays a critical role in SPIN6 and SDS2-mediated defense responses. BAG4 and SPL35 are positive regulators of programmed cell death (PCD), and excessive accumulation can lead to PCD. They are degraded by an E3 ubiquitin ligase. The NPR1 is degraded by enhancing the association between NPR1 and CUL3a, which disrupts the salicylic acid (SA)- and jasmonic acid (JA)-mediated synergistic immunity in rice.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| SPL28, PSL50 | Os01g0703600 | A subunit of clathrin-associated adaptor protein | Magnaporthe oryzae and Xanthomonas oryzae (Xoo) | Qiao et al, |
| NPR1, NH1 | Os01g0194300 | Salicylic acid receptor | M. oryzae and Xoo | Li et al, |
| LMR, LRD6-6 | Os06g0130000 | ATP; AAA ATPase | M. oryzae and Xoo | Fekih et al, |
| SPIN6 | Os07g0658300 | Rho GTPase activating protein | M. oryzae and Xoo | Liu et al, |
| SPL11 | Os12g0570000 | E3 ubiquitin ligase | M. oryzae and Xoo | Liu et al, |
| EBR1 | Os05g0279400 | E3 ubiquitin ligase | M. oryzae and Xoo | You et al, |
| BAG4 | Os01g0831200 | BAG protein; Molecular chaperone regulatory proteins | M. oryzae and Xoo | You et al, |
| CUL3a | Os02g0746000 | Cullin protein | M. oryzae and Xoo | Liu et al, |
| SDS2 | Os01g0783800 | Receptor-like kinase | M. oryzae | Fan et al, |
| SCYL2 | Os01g0616100 | Clathrin-coated vesicle components | Xoo | Yao et al, |
Table 1. Necrotic lesion genes are involved in mitogen-activated protein kinase signaling and ubiquitination pathways and clathrin-mediated vesicle transport pathway.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| SPL28, PSL50 | Os01g0703600 | A subunit of clathrin-associated adaptor protein | Magnaporthe oryzae and Xanthomonas oryzae (Xoo) | Qiao et al, |
| NPR1, NH1 | Os01g0194300 | Salicylic acid receptor | M. oryzae and Xoo | Li et al, |
| LMR, LRD6-6 | Os06g0130000 | ATP; AAA ATPase | M. oryzae and Xoo | Fekih et al, |
| SPIN6 | Os07g0658300 | Rho GTPase activating protein | M. oryzae and Xoo | Liu et al, |
| SPL11 | Os12g0570000 | E3 ubiquitin ligase | M. oryzae and Xoo | Liu et al, |
| EBR1 | Os05g0279400 | E3 ubiquitin ligase | M. oryzae and Xoo | You et al, |
| BAG4 | Os01g0831200 | BAG protein; Molecular chaperone regulatory proteins | M. oryzae and Xoo | You et al, |
| CUL3a | Os02g0746000 | Cullin protein | M. oryzae and Xoo | Liu et al, |
| SDS2 | Os01g0783800 | Receptor-like kinase | M. oryzae | Fan et al, |
| SCYL2 | Os01g0616100 | Clathrin-coated vesicle components | Xoo | Yao et al, |
Fig. 3. Reactive oxygen species, clathrin-mediated vesicle transport, and other signaling pathways regulate necrotic lesion formation. WRK26, MED16, and NBL3 activate resistance genes, CNGC9 regulates resistance gene activation by regulating Ca2+ concentration, and RLR1 works with WRKY19 to activate resistance gene. SPL28- SCYL2 and LMR participate in the defense response by mediating vesicle transport. DjA9 and DRP1E affect mitochondrial size, thereby affecting reactive oxygen species, ultimately participating in immune regulation. LSL1 interacts with PsaD and PAP10 to affect chloroplast homeostasis, and RLIN1 and LC7 also participate in disease resistance by affecting chloroplast homeostasis. SPL7 regulates resistance by inhibiting NADPH enzyme activity, Pti1a inhibits RAR1 activity, while RMC and RLS1 both participate in disease resistance by inhibiting self-immunity. LML1 and SPL33 interact in the endoplasmic reticulum, thereby affecting protein folding. ‘→’ symbol indicates activation or next step, and ‘├’ symbol indicates inhibition.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| LSD1, LOL1 | Os08g0159500 | Zinc finger protein | Magnaporthe oryzae | Wang et al, |
| OsHsfA4d, SPL7 | Os05g0530400 | Heat shock transcription factors | M. oryzae and Xanthomonas oryzae (Xoo) | Hoang et al, |
| RLIN1, LLM1 | Os04g0610800 | Coproporphyrinogen III oxidase | Xoo | Sun et al, |
| lc7, SPL32, Fd-GOGAT1, ABC1 | Os07g0658400 | Glutamate synthase | Xoo | Chen et al, |
| SPL33 | Os01g0116600 | Eef1a-like protein; Eukaryotic translation extension factor alpha protein | M. oryzae and blight | Wang et al, |
| LMM5 | Os04g0596500 | Eef1a-like protein | M. oryzae and Xoo | Zhao et al, |
| LML1 | Os04g0659900 | Eukaryotic release factor 1 albumen | M. oryzae and Xoo | Qin et al, |
| spl26 | Os07g0141200 | Protein kinase | M. oryzae and Xoo | Chen et al, |
| SPL35 | Os03g0205000 | CUE domain protein | M. oryzae and Xoo | Ma et al, |
| LMM24 | Os03g0364400 | Receptor-like cytoplasmic kinase | M. oryzae | Zhang et al, |
| NRAMP1 | Os07g0258400 | Metal ion transporter; Natural resistance- associated macrophage proteins. | M. oryzae and Xoo | Chang et al, |
| SPL36 | Os12g0182300 | Receptor-like protein kinase | Xoo | Rao et al, |
| LSL1/GRDP1 | Os11g0621300 | Glycine-enriched domain proteins | M. oryzae and Xoo | Zhao et al, |
Table 2. Necrotic lesion genes are involved in reactive oxygen species pathways.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| LSD1, LOL1 | Os08g0159500 | Zinc finger protein | Magnaporthe oryzae | Wang et al, |
| OsHsfA4d, SPL7 | Os05g0530400 | Heat shock transcription factors | M. oryzae and Xanthomonas oryzae (Xoo) | Hoang et al, |
| RLIN1, LLM1 | Os04g0610800 | Coproporphyrinogen III oxidase | Xoo | Sun et al, |
| lc7, SPL32, Fd-GOGAT1, ABC1 | Os07g0658400 | Glutamate synthase | Xoo | Chen et al, |
| SPL33 | Os01g0116600 | Eef1a-like protein; Eukaryotic translation extension factor alpha protein | M. oryzae and blight | Wang et al, |
| LMM5 | Os04g0596500 | Eef1a-like protein | M. oryzae and Xoo | Zhao et al, |
| LML1 | Os04g0659900 | Eukaryotic release factor 1 albumen | M. oryzae and Xoo | Qin et al, |
| spl26 | Os07g0141200 | Protein kinase | M. oryzae and Xoo | Chen et al, |
| SPL35 | Os03g0205000 | CUE domain protein | M. oryzae and Xoo | Ma et al, |
| LMM24 | Os03g0364400 | Receptor-like cytoplasmic kinase | M. oryzae | Zhang et al, |
| NRAMP1 | Os07g0258400 | Metal ion transporter; Natural resistance- associated macrophage proteins. | M. oryzae and Xoo | Chang et al, |
| SPL36 | Os12g0182300 | Receptor-like protein kinase | Xoo | Rao et al, |
| LSL1/GRDP1 | Os11g0621300 | Glycine-enriched domain proteins | M. oryzae and Xoo | Zhao et al, |
Fig. 4. Necrotic lesion genes are involved in hormone signaling pathways. NPR1 is involved in rice defense response by CUL3a ubiquitination degration and hormone level regulation. ICS1 is a key enzyme in the salicylic acid (SA) synthesis pathway and is regulated by WRKY6. WRKY6 also activates pathogenic resistance genes to participate in defense response by activating WRKY45 and WRKY47. SSI2, WED, PELOTA, and GF14E contribute to disease resistance by influencing salicylic acid content. HPL3 affects rice disease resistance by inhibiting linolenic acid. SPL3 and GF14E directly inhibit the jasmonic acid (JA) participation in rice defense response. EDR1 and SPL40 participate in the defense response by influencing SA and JA content.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| Salicylic acid signaling pathway | ||||
| SSI2 | Os01g0919900 | Fatty acid dehydrogenase | Magnaporthe oryzae and Xanthomonas oryzae (Xoo) | Jiang et al, |
| NPR1, NH1 | Os01g0194300 | Salicylic acid receptor | M. oryzae and Xoo | Li et al, |
| WRKY6 | Os03g0798500 | WRKY transcriptional factor | M. oryzae | Choi et al, |
| CUL3a | Os02g0746000 | Cullin protein | M. oryzae and Xoo | Liu et al, |
| PELOTA | Os04g0659900 | Eukaryotic translation release factor | Xoo | Zhang et al, |
| WED | Os11g0646300 | NLR protein | Xoo | Tang et al, |
| Jasmonic acid signaling pathway | ||||
| HPL3, cea62 | Os02g0110200 | Hydroperoxide lyase | Xoo | Liu et al, |
| LLB, SPL3, MTS1 | Os07g0247100 | Leucine carboxymethyltransferase | M. oryzae and Xoo | Tamiru et al, |
| Salicylic acid and jasmonic acid signaling pathways | ||||
| SPL3, EDR1, ACDR1, MAPKKK1 | Os03g0160100 | Mitogen-activated protein kinase kinase kinase kinase | M. oryzae | Shen et al, |
| GF14e | Os02g0580300 | 14-3-3 protein | Xoo and corn sheath blight | Liu et al, |
| SPL40 | Os05g0312000 | Structural components of ribosomes | Xoo | Sathe et al, |
| Other hormone signaling pathway | ||||
| SL, ELL1, T5H, CYP71P1, CYP71A1 | Os12g0268000 | Tryptamine hydroxylase; Cytochrome P450 monooxygenase | M. oryzae and Xoo | Fujiwara et al, et al, 2020; Cui et al, |
| SPL29, UAP1 | Os08g0206900 | Uridine diphosphate N-acetylglucosamine pyrophosphorylase | Xoo | Wang et al, |
Table 3. Necrotic lesion genes are involved in hormonal pathways.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| Salicylic acid signaling pathway | ||||
| SSI2 | Os01g0919900 | Fatty acid dehydrogenase | Magnaporthe oryzae and Xanthomonas oryzae (Xoo) | Jiang et al, |
| NPR1, NH1 | Os01g0194300 | Salicylic acid receptor | M. oryzae and Xoo | Li et al, |
| WRKY6 | Os03g0798500 | WRKY transcriptional factor | M. oryzae | Choi et al, |
| CUL3a | Os02g0746000 | Cullin protein | M. oryzae and Xoo | Liu et al, |
| PELOTA | Os04g0659900 | Eukaryotic translation release factor | Xoo | Zhang et al, |
| WED | Os11g0646300 | NLR protein | Xoo | Tang et al, |
| Jasmonic acid signaling pathway | ||||
| HPL3, cea62 | Os02g0110200 | Hydroperoxide lyase | Xoo | Liu et al, |
| LLB, SPL3, MTS1 | Os07g0247100 | Leucine carboxymethyltransferase | M. oryzae and Xoo | Tamiru et al, |
| Salicylic acid and jasmonic acid signaling pathways | ||||
| SPL3, EDR1, ACDR1, MAPKKK1 | Os03g0160100 | Mitogen-activated protein kinase kinase kinase kinase | M. oryzae | Shen et al, |
| GF14e | Os02g0580300 | 14-3-3 protein | Xoo and corn sheath blight | Liu et al, |
| SPL40 | Os05g0312000 | Structural components of ribosomes | Xoo | Sathe et al, |
| Other hormone signaling pathway | ||||
| SL, ELL1, T5H, CYP71P1, CYP71A1 | Os12g0268000 | Tryptamine hydroxylase; Cytochrome P450 monooxygenase | M. oryzae and Xoo | Fujiwara et al, et al, 2020; Cui et al, |
| SPL29, UAP1 | Os08g0206900 | Uridine diphosphate N-acetylglucosamine pyrophosphorylase | Xoo | Wang et al, |
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| SPL18 | Os10g0195600 | Acyltransferase | Magnaporthe oryzae and Xanthomonas oryzae (Xoo) | Mori et al, |
| PTI1A, TTM1 | Os05g0135800 | Protein kinase | M. oryzae and Xoo | Takahashi et al, |
| PLDβ1 | Os10g0524400 | Phospholipase D | M. oryzae and Xoo | Yamaguchi et al, |
| NLS1 | Os11g0249000 | CC-NB-LRR protein | Xoo | Tang et al, |
| SPL5, SF3b3, SL5 | Os07g0203700 | Splicing factor 3b subunit | M. oryzae and Xoo | Chen et al, |
| LMS | Os02g0639000 | Double-stranded RNA binding domain | M. oryzae | Undan et al, |
| CslF6 | Os08g0160500 | Cellulose-like synthase | Xoo | Vega-Sánchez et al, |
| DPF, bHLH025 | Os01g0196300 | bHLH transcription factor | M. oryzae | Yamamura et al, |
| WAK25 | Os03g0225700 | Cell wall associated receptor-like kinases | M. oryzae and Xoo | Harkenrider et al, |
| DRP1E | Os09g0572900 | Motor protein | M. oryzae and Xoo | Li et al, |
| SPL30, ACL-A2, ACLA-3 | Os12g0566300 | ATP-citrate lyase | Xoo | Ruan et al, |
| CNGC9, CDS1 | Os09g0558300 | Cyclic nucleotide-gated ion channel | M. oryzae | Wang et al, |
| RLR1 | Os10g0163040 | CC-NB-LRR protein | M. oryzae and Xoo | Du et al, |
| NBL3 | Os03g0159700 | Triangular pentapeptide repeat protein | M. oryzae and Xoo | Qiu et al, |
| RBL1 | Os01g0758400 | CDP-DAG | M. oryzae and Xoo | Sha et al, |
| RLS1 | Os02g0203500 | NB-ARM protein | Xoo | Wang et al, |
| SPL38, MED16, SFR6 | Os10g0498700 | RNA polymerase II transcriptional mediator subunit | M. oryzae and Xoo | Zhang P et al, |
Table 4. Necrotic lesion genes are involved in other signaling pathways.
| Gene name | Accession number | Protein function | Disease resistance | Reference |
|---|---|---|---|---|
| SPL18 | Os10g0195600 | Acyltransferase | Magnaporthe oryzae and Xanthomonas oryzae (Xoo) | Mori et al, |
| PTI1A, TTM1 | Os05g0135800 | Protein kinase | M. oryzae and Xoo | Takahashi et al, |
| PLDβ1 | Os10g0524400 | Phospholipase D | M. oryzae and Xoo | Yamaguchi et al, |
| NLS1 | Os11g0249000 | CC-NB-LRR protein | Xoo | Tang et al, |
| SPL5, SF3b3, SL5 | Os07g0203700 | Splicing factor 3b subunit | M. oryzae and Xoo | Chen et al, |
| LMS | Os02g0639000 | Double-stranded RNA binding domain | M. oryzae | Undan et al, |
| CslF6 | Os08g0160500 | Cellulose-like synthase | Xoo | Vega-Sánchez et al, |
| DPF, bHLH025 | Os01g0196300 | bHLH transcription factor | M. oryzae | Yamamura et al, |
| WAK25 | Os03g0225700 | Cell wall associated receptor-like kinases | M. oryzae and Xoo | Harkenrider et al, |
| DRP1E | Os09g0572900 | Motor protein | M. oryzae and Xoo | Li et al, |
| SPL30, ACL-A2, ACLA-3 | Os12g0566300 | ATP-citrate lyase | Xoo | Ruan et al, |
| CNGC9, CDS1 | Os09g0558300 | Cyclic nucleotide-gated ion channel | M. oryzae | Wang et al, |
| RLR1 | Os10g0163040 | CC-NB-LRR protein | M. oryzae and Xoo | Du et al, |
| NBL3 | Os03g0159700 | Triangular pentapeptide repeat protein | M. oryzae and Xoo | Qiu et al, |
| RBL1 | Os01g0758400 | CDP-DAG | M. oryzae and Xoo | Sha et al, |
| RLS1 | Os02g0203500 | NB-ARM protein | Xoo | Wang et al, |
| SPL38, MED16, SFR6 | Os10g0498700 | RNA polymerase II transcriptional mediator subunit | M. oryzae and Xoo | Zhang P et al, |
Fig. 5. Mining and application potential of necrotic lesion genes. In the process of agricultural production, necrotic lesion mutants can reduce the use of pesticides and save on environmental costs because of their high resistance characteristics. However, it is difficult to implement them in agricultural production under normal conditions. We need to analyze the disease resistance mechanism of necrotic lesion genes using current molecular technology, establish germplasm resource banks through high-throughput genome sequencing, genome-wide association studies (GWAS), and QTL mapping. By integrating gene editing with traditional breeding methods, we can create a new balance of ‘high-yield and high-resistance’.
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