Rice Science ›› 2025, Vol. 32 ›› Issue (1): 32-43.DOI: 10.1016/j.rsci.2024.12.003
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Hao Zhiqi1,#, Wang Tingyi1,#, Chen Dongdong1, Shen Lan1, Zhang Guangheng1,3, Qian Qian1,2, Zhu Li1,3(
)
Received:2024-07-29
Accepted:2024-12-10
Online:2025-01-28
Published:2025-03-25
Contact:
Zhu Li
About author:First author contact:#These authors contributed equally to this work
Hao Zhiqi, Wang Tingyi, Chen Dongdong, Shen Lan, Zhang Guangheng, Qian Qian, Zhu Li. Leucine-Rich Repeat Protein Family Regulates Stress Tolerance and Development in Plants[J]. Rice Science, 2025, 32(1): 32-43.
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| Type | Gene | Function | LRR location | No. of LRRs | Plant origin | Reference |
|---|---|---|---|---|---|---|
| LRR-RLK | ERECTA | Transpiration efficiency | N-terminus | 18 | Arabidopsis thaliana | Masle et al, |
| OsSIK1 | Drought and salt stress | N-terminus | 16 | Oryza sativa | Ouyang et al, | |
| FLS2 | Signaling activation; Mediated immunity | N-terminus | 25 | A. thaliana | Cao et al, | |
| PXC1 | Secondary cell wall formation; Tracheary element differentiation inhibitory factor-phloem intercalated with xylem/TDIF receptor-WOX4 signaling | N-terminus | 4 | A. thaliana | Wang J H et al, | |
| LIK1 | Immune responses | N-terminus | 10 | A. thaliana | Le et al, | |
| OsGIRL1 | Abiotic stress | N-terminus | - | O. sativa | Park et al, | |
| NIK1 | Geminivirus resistance | N-terminus | 4 | A. thaliana | Zorzatto et al, | |
| OsWAK25 | Biological stress | N-terminus | - | O. sativa | Harkenrider et al, | |
| MRK1 | Temperature stress; Resistance to bacterial disease | N-terminus | 5 | Solanum lycopersicum | Ma et al, | |
| RINRK1 | Nodulation factor signaling; Rhizobia infection | N-terminus | 3 | Lotus japonicus | Li X L et al, | |
| ZmRLK7 | Enlarges organ and seed size | N-terminus | 10 | Zea mays | He et al, | |
| HSL3 | Drought stress | N-terminus | 18 | A. thaliana | Liu et al, | |
| MtCTLK1 | Cold tolerance | N-terminus | 3 | Medicago truncatula | Geng et al, | |
| OsCERK1 | Chitin signaling | N-terminus | - | O. sativa | Yang et al, | |
| OsBAK1 | Immune regulation | N-terminus | 4 | O. sativa | Duan et al, | |
| LRR-RLP | HcrVf2 | Resistance to Venturia inaequalis | N-terminus | 27 | Malus floribunda | Belfanti et al, |
| ReMAX | Perception of enigmatic MAMP protein of Xanthomonas | N-terminus | 27 | A. thaliana | Jehle et al, | |
| RFO2 | Resistance to Fusarium oxysporum | N-terminus | 16 | A. thaliana | Shen and Diener, | |
| VE1 | Resistance to Verticillium dahliae and V. albo-atrum | N-terminus | 30 | S. lycopersicum | Nazar et al, | |
| OsRLP1 | Resistance to rice black-streaked dwarf virus | N-terminus | 26 | O. sativa | Zhang H H et al, | |
| COG1 | Cold stress response | N-terminus | 17 | O. sativa | Xia et al, | |
| NBS-LRR | RPM1 | Resistance to Pseudomonas syringae | C-terminus | 9 | A. thaliana | Tornero et al, |
| Rxo1/Rba1 | Non-host resistance and resistance to pathogens | C-terminus | 9 | Z. mays | Zhao et al, | |
| BNT1 | Alters plant stress hormone levels | C-terminus | 11 | A. thaliana | Sarazin et al, | |
| Pm21 | Confers powdery mildew resistance | C-terminus | 6 | Haynaldia villosa | Xing et al, | |
| OsPi304 | Cold stress response | C-terminus | - | O. sativa | Yang et al, | |
| GhDSC1 | Resistance to Verticillium wilt | C-terminus | 4 | Gossypium hirsutum | Li T G et al, | |
| Roq1 | Interacts with Xanthomonas outer protein Q and triggers hypersensitive cell death | C-terminus | 24 | Nicotiana benthamiana | Martin et al, | |
| L5 | Induces cell death and self-association | C-terminus | 2 | A. thaliana | Huang et al, | |
| SNC1 | Immune activation | C-terminus | 19 | A. thaliana | Jia et al, | |
| MdTNL1 | Resistance to Glomerella leaf spot | C-terminus | 7 | M. domestica | Lv et al, | |
| RppM | Resistance to Southern Corn Rust | C-terminus | 17 | Z. mays | Wang S et al, | |
| LRX | LRX1 | Cell wall formation | N-terminus | 8 | A. thaliana | Draeger et al, |
| LRX2 | Cell wall formation | N-terminus | 8 | A. thaliana | Draeger et al, | |
| LRX3 | Regulates growth and salt tolerance | N-terminus | 8 | A. thaliana | Zhao et al, | |
| LRX4 | Regulates growth and salt tolerance | N-terminus | 8 | A. thaliana | Zhao et al, | |
| LRX5 | Regulates growth and salt tolerance | N-terminus | 8 | A. thaliana | Zhao et al, | |
| PGIP | AtPGIP1 | Resistance to Botrytis cinerea | C-terminus | 7 | A. thaliana | Ferrari et al, |
| GmPGIP1 | Resistance to Fusarium moniliforme | C-terminus | 9 | Glycine max | Maulik et al, | |
| PvPGIP1 | Resistance to F. moniliforme | C-terminus | 8 | Phaseolus vulgaris | Maulik et al, | |
| OsPGIP2 | Polygalacturonase inhibition | C-terminus | 6 | O. sativa | Chen et al, | |
| OsPGIP1 | Bacterial leaf streak tolerance | C-terminus | 7 | O. sativa | Wu et al, | |
| OsPGIP4 | Bacterial leaf streak | C-terminus | 8 | O. sativa | Wu et al, | |
| VrPGIP2 | Resistance to bruchids | C-terminus | 8 | Vigna radiata | Zhang Q et al, |
Table 1. Selected members of LRR protein family in plants.
| Type | Gene | Function | LRR location | No. of LRRs | Plant origin | Reference |
|---|---|---|---|---|---|---|
| LRR-RLK | ERECTA | Transpiration efficiency | N-terminus | 18 | Arabidopsis thaliana | Masle et al, |
| OsSIK1 | Drought and salt stress | N-terminus | 16 | Oryza sativa | Ouyang et al, | |
| FLS2 | Signaling activation; Mediated immunity | N-terminus | 25 | A. thaliana | Cao et al, | |
| PXC1 | Secondary cell wall formation; Tracheary element differentiation inhibitory factor-phloem intercalated with xylem/TDIF receptor-WOX4 signaling | N-terminus | 4 | A. thaliana | Wang J H et al, | |
| LIK1 | Immune responses | N-terminus | 10 | A. thaliana | Le et al, | |
| OsGIRL1 | Abiotic stress | N-terminus | - | O. sativa | Park et al, | |
| NIK1 | Geminivirus resistance | N-terminus | 4 | A. thaliana | Zorzatto et al, | |
| OsWAK25 | Biological stress | N-terminus | - | O. sativa | Harkenrider et al, | |
| MRK1 | Temperature stress; Resistance to bacterial disease | N-terminus | 5 | Solanum lycopersicum | Ma et al, | |
| RINRK1 | Nodulation factor signaling; Rhizobia infection | N-terminus | 3 | Lotus japonicus | Li X L et al, | |
| ZmRLK7 | Enlarges organ and seed size | N-terminus | 10 | Zea mays | He et al, | |
| HSL3 | Drought stress | N-terminus | 18 | A. thaliana | Liu et al, | |
| MtCTLK1 | Cold tolerance | N-terminus | 3 | Medicago truncatula | Geng et al, | |
| OsCERK1 | Chitin signaling | N-terminus | - | O. sativa | Yang et al, | |
| OsBAK1 | Immune regulation | N-terminus | 4 | O. sativa | Duan et al, | |
| LRR-RLP | HcrVf2 | Resistance to Venturia inaequalis | N-terminus | 27 | Malus floribunda | Belfanti et al, |
| ReMAX | Perception of enigmatic MAMP protein of Xanthomonas | N-terminus | 27 | A. thaliana | Jehle et al, | |
| RFO2 | Resistance to Fusarium oxysporum | N-terminus | 16 | A. thaliana | Shen and Diener, | |
| VE1 | Resistance to Verticillium dahliae and V. albo-atrum | N-terminus | 30 | S. lycopersicum | Nazar et al, | |
| OsRLP1 | Resistance to rice black-streaked dwarf virus | N-terminus | 26 | O. sativa | Zhang H H et al, | |
| COG1 | Cold stress response | N-terminus | 17 | O. sativa | Xia et al, | |
| NBS-LRR | RPM1 | Resistance to Pseudomonas syringae | C-terminus | 9 | A. thaliana | Tornero et al, |
| Rxo1/Rba1 | Non-host resistance and resistance to pathogens | C-terminus | 9 | Z. mays | Zhao et al, | |
| BNT1 | Alters plant stress hormone levels | C-terminus | 11 | A. thaliana | Sarazin et al, | |
| Pm21 | Confers powdery mildew resistance | C-terminus | 6 | Haynaldia villosa | Xing et al, | |
| OsPi304 | Cold stress response | C-terminus | - | O. sativa | Yang et al, | |
| GhDSC1 | Resistance to Verticillium wilt | C-terminus | 4 | Gossypium hirsutum | Li T G et al, | |
| Roq1 | Interacts with Xanthomonas outer protein Q and triggers hypersensitive cell death | C-terminus | 24 | Nicotiana benthamiana | Martin et al, | |
| L5 | Induces cell death and self-association | C-terminus | 2 | A. thaliana | Huang et al, | |
| SNC1 | Immune activation | C-terminus | 19 | A. thaliana | Jia et al, | |
| MdTNL1 | Resistance to Glomerella leaf spot | C-terminus | 7 | M. domestica | Lv et al, | |
| RppM | Resistance to Southern Corn Rust | C-terminus | 17 | Z. mays | Wang S et al, | |
| LRX | LRX1 | Cell wall formation | N-terminus | 8 | A. thaliana | Draeger et al, |
| LRX2 | Cell wall formation | N-terminus | 8 | A. thaliana | Draeger et al, | |
| LRX3 | Regulates growth and salt tolerance | N-terminus | 8 | A. thaliana | Zhao et al, | |
| LRX4 | Regulates growth and salt tolerance | N-terminus | 8 | A. thaliana | Zhao et al, | |
| LRX5 | Regulates growth and salt tolerance | N-terminus | 8 | A. thaliana | Zhao et al, | |
| PGIP | AtPGIP1 | Resistance to Botrytis cinerea | C-terminus | 7 | A. thaliana | Ferrari et al, |
| GmPGIP1 | Resistance to Fusarium moniliforme | C-terminus | 9 | Glycine max | Maulik et al, | |
| PvPGIP1 | Resistance to F. moniliforme | C-terminus | 8 | Phaseolus vulgaris | Maulik et al, | |
| OsPGIP2 | Polygalacturonase inhibition | C-terminus | 6 | O. sativa | Chen et al, | |
| OsPGIP1 | Bacterial leaf streak tolerance | C-terminus | 7 | O. sativa | Wu et al, | |
| OsPGIP4 | Bacterial leaf streak | C-terminus | 8 | O. sativa | Wu et al, | |
| VrPGIP2 | Resistance to bruchids | C-terminus | 8 | Vigna radiata | Zhang Q et al, |
Fig. 1. Structures of leucine-rich repeat (LRR) receptor-like kinases (LRR-RLKs) and LRR receptor-like proteins (LRR-RLPs). A, Structural diagram of LRR-RLKs, which comprise an LRR domain, a transmembrane domain, and a kinase domain. B, Structural diagram of LRR-RLPs, which lack a kinase domain. C, Structure of Toll/interleukin-1 receptor (TIR) nucleotide-binding site LRR proteins (NBS-LRRs) (TIR-NBS-LRRs or TNLs). D, Structure of coiled-coil (CC) NBS-LRR (CC-NBS-LRRs or CNLs). E, Structure of LRR-extensin proteins (LRXs), which contain a signal peptide, a variable region, and an LRR domain, along with an extensin domain at the C-terminus. F, Schematic diagram of polygalacturonase-inhibiting proteins (PGIPs).
Fig. 2. Mechanisms of plant leucine-rich repeats (LRRs) in different stress signal transduction pathways. LRR family proteins are widely involved in various signal transduction processes in plants. Both the LRR receptor-like kinase (LRR-RLK) BAK1 and droopy leaf1 (DPY1) are involved in the brassinosteroid (BR) signaling pathway. DPY1 plays a crucial role in determining leaf droopiness by controlling BR signaling output. It is also important for sensing changes in osmotic potential and for intracellular signal transduction. Moreover, BAK1 has important function in the immune response. BAK1 interacts with FLS2 to enhance the generation of reactive oxygen species (ROS) and regulate stomatal closure. This interaction is crucial in the early defense of plants against bacteria. BAK1 also cooperates with other LRR-RLK receptors to regulate pathogen-associated defense responses. BRI1 and FLS2 phosphorylate different sites on bri1-suppressor1 (BSU1) phosphatase, which regulates the activity of downstream glycogen synthase kinase 3 (GSK3) and mitogen-activated protein kinase (MAPK) signaling pathways, respectively. The nucleotide-binding site and LRR receptor (NLR) protein ZAR1 and Sr35 resistosome can insert into lipid bilayer membranes to form cation channels with Ca2+ ion permeability, thereby performing immune response functions. The LRR-RLK hydrogen-peroxide-induced Ca2+ increase 1 (HPCA1) functions as a cellular H2O2 sensor that affects the activation of Ca2+ channels in guard cells via H2O2 signaling, the affecting the opening and closing of the stomata. In rice, the LRR-RLK ALR1 (aluminum resistance1) confers resistance to aluminum (Al) toxicity through an integrated Al-triggered signaling pathway. ALR1 binds Al ions, and its cytoplasmic domain recruits the BAK1 co-receptor kinase, promoting ALR1-dependent phosphorylation of RbohD by NADPH oxidase, thereby enhancing ROS production. The LRR-RLK ERECTA-LIKE 1 (ERL1) and ERECTA-LIKE 2 (ERL2) are involved in the gibberellin (GA) signaling pathway, affecting the expression of downstream GA reporter genes. The rice LRR-RLP Chilling-tolerance in Gengdao/japonica rice 1 (COG1) forms a complex with OsSERL2, further activate OsSERL2 perception of cold-stress signals in the plasma membrane. As a signaling hub, feronia (FER) regulates a variety of biotic and abiotic signaling pathways, enabling plants to respond to environmental changes and regulate growth and development. FER interacts with the target of rapamycin (TOR) protein in the TOR pathway, activating downstream components that trigger root hair growth under low-nutrient conditions. Additionally, FER cooperates with BRI1 to regulate plant cell growth, particularly during root and stem development.
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