Deciphering Rice Lesion Mimic Mutants to Understand Molecular Network Governing Plant Immunity and Growth

doi:10.1016/j.rsci.2020.05.004

Abstract

Abstract:

Plant lesion mimic mutants (lmms) generally possess autoimmunity and hypersensitive response (HR)-like cell death in the absence of biotic or abiotic stress. They have attracted much attention because they are useful tools for deciphering the interaction between defense signaling and growth. Recent studies have identified more than 30 lmms involved in the plant immune response and cell death in rice. Genes underlying these lmms, coding for diverse types of proteins, mainly regulate transcription, protein translation and modification, vesicular trafficking and catalyzation of metabolism. Here, we presented an overview of the most recent advances on the study of lmms in rice and proposed a perspective on potential utilization of LMM genes in agriculture.

Key words: lesion mimic mutant, autoimmunity, cell death, growth regulation, rice

Xiaobo Zhu, Mu Ze, Mawsheng Chern, Xuewei Chen, Jing Wang. Deciphering Rice Lesion Mimic Mutants to Understand Molecular Network Governing Plant Immunity and Growth[J]. Rice Science, 2020, 27(4): 278-288.

Figures/Tables 2

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Year	Mutant/ gene name	Genetic mode	Gene ID	Protein encoded	Protein localization	Disease resistance	Effects on growth and development	Possible mechanisms involved	References
2002	spl7	Single recessive	LOC_Os05g45410	Heat stress transcription factor	NS	Er to RB.	NS	NS	Kojo et al, 2006, Yamanouchi et al, 2002
2005	oslsd1	Single recessive	LOC_Os08g06280	Zinc finger protein	Nucleus	Both RNAi and over expression conferred resistance against RB.	Overexpression accelerate callus differentiation, present dark green leaf color and promote seeds germination.	OsLOL1 interacted with OsbZIP58 to regulate the expression of the SOD1 and OsKO2 genes.	Wang et al, 2005
2005	NH1/OsNPR1	Single dominant	LOC_Os01g09800	BTB domain and ankyrin repeat region contained protein.	Cytosol and nucleus	Er to BB but susceptible to WBPH.	Similar to wild type.	Regulates the SA mediated resistance.	Chern et al, 2005, Yuan et al, 2007
2012	oslms	Single recessive	LOC_Os02g42600	Two double-stranded RNA binding motifs contain protein.	NS	Er to RB	Sensitive to cold stress.	NS	Undan et al, 2012
2009	spl5/ossl5	Single recessive	LOC_Os07g10390	A putative splicing factor 3b subunit 3 (SF3b3).	NS	Er to both RB and BB.	Adversely impacted.	Negative regulatory factor activating the serotonin metabolic pathway.	Chen et al, 2012, Jin et al, 2015, Ge et al, 2015
2016	lmm5	Two recessive	LOC_Os01g02720; LOC_Os04g50870	Eukaryotic translation elongation factor 1A (eEF1A)-like protein.	NS	Er to both RB and BB	NS	NS	Zhao et al, 2017
2016	spl33	Single recessive	LOC_Os01g02720	Eukaryotic translation elongation factor 1A (eEF1A)-like protein.	ER	Er to both RB and BB	NS	NS	Wang et al, 2017
2018	lml1/ spl^HM47	Single recessive	LOC_Os04g56480	Eukaryotic release factor 1 (eRF1).	ER and plasma membrane.	Er to both RB and BB.	Growth delay and smaller organs.	Forms a functional complex with SPL33/LMM5.1.	Qin et al, 2018, Zhang et al, 2018
2004	spl11	Single recessive	LOC_Os12g38210	U-box domain and an armadillo (ARM) repeat domain contained E3 ubiquitin ligase.	NS	Er to both RB and BB	Delayed flowering under long-day conditions.	SPL11 interacts with and mediated ubiquitination of SPIN6 to regulate OsRac1 associated defensome system; SPL11 also interacts with and ubiquitination SDS2 to regulate the RLCK118-OsRbohB mediated immunity. SPL11 negatively regulates SPIN1 to control flowering time.	Fan et al, 2018, Liu et al, 2012a, Liu et al, 2015, Vega-Sanchez et al, 2008, Zeng et al, 2004
2016	ebr1	Single recessive	LOC_Os05g19970	RING-type E3 ligase.	NS	Er to both RB and BB.	NS	EBR1 targets OsBAG4, a BAG protein promoting immunity and antimicrobial defense, to fine-tune immune homeostasis.	You et al, 2016
2017	oscul3a	Single recessive	LOC_Os02g51180	Cullin3-based RING E3 ubiquitin ligases (CRL3) component, CUL3a.	NS	Er to both RB and BB	NS	OsCUL3a interacts with and degrades OsNPR1.	Liu et al, 2017
2019	spl35	Single recessive	LOC_Os03g10750	CUE domain-containing protein.	Cytosol, ER and punctate compartment(s).	Er to both RB and BB	Adversely impacted	Involved in the mono-ubiquitination and vesicular trafficking pathways.	Ma et al, 2019
2011	spl3/osedr1/osacdr1	Single recessive	LOC_Os03g06410	Mitogen-Activated Protein Kinase Kinase Kinase	Nucleus	The osedr1 mutant possessed enhanced resistance to BB; OsAcdr1 over expression enhance RB resistance.	Delayed leaf senescence	OsEDR1 negatively regulates resistance via activation of ET biosynthesis; OsACDR1-OE plants accumulate phenolic compounds and secondary metabolites, and express enhanced levels of defense-related marker genes.	Wang et al, 2015b, Shen et al, 2011, Kim et al, 2009
2014	ospti1a/ttm1	Single recessive	LOC_Os05g04520	Protein kinase	Plasma membrane	Er to both RB and BB	Stunted growth	Regulates RAR1-dependent defense responses.	Matsui et al, 2015, Takahashi et al, 2007
2017	als1/lil1	Single semi-dominant	LOC_Os07g30510	Cysteine-rich receptor-like kinase (CRK).	Plasma membrane	Er to RB	NS	Activation of a common SA-, JA- and NH1-mediated defense response.	Du et al, 2019, Zhou et al, 2017
2018	sles	Single recessive	LOC_Os07g25680	Mitogen-Activated Protein Kinase Kinase Kinase	NS	Er to RB	Adversely impacted	NS	Lee et al, 2018
2019	psl	Single recessive	LOC_Os12g42420	Core 2/I branching beta-1,6-Nacetylglucosaminyl transferase	NS	NS	Adversely impacted	NS	Ke et al, 2019
2010	spl28	Single recessive	LOC_Os01g50770	Clathrin-associated adaptor protein complex 1, medium subunit μ1 (AP1M1)	Golgi	Er to both RB and BB	Adversely impacted.	Involved in post-Golgi trafficking pathway, accumulation of antimicrobial compounds.	Qiao et al, 2010
2015	lmr/lrd6-6/spl4	Single recessive	LOC_Os06g03940	AAA ATPase	Chloroplast, MVBs	Er to both RB and BB	Delayed leaf yellowing and adversely impacted.	Modulating MVBs-mediated vesicular trafficking and activating the biosynthesis of antimicrobial compounds.	Zhu et al, 2016, Song et al, 2018, Fekih et al, 2015
2015	rls2	Single recessive	LOC_Os04g58880	EXO70A1	Punctate signals both on the PM and within the nucleus	DR	NS	NS	Tu et al, 2015
2017	ossec3a	Single recessive	LOC_Os03g42750	Member of the exocyst complex, SEC3A.	Punctate distribution on the plasma membrane	Er to RB	Adversely impacted	OsSEC3A interacted with rice SNAP25-type t-SNARE protein OsSNAP32, which is involved in rice blast resistance.	Ma et al, 2018
2007	spl18	Single dominant	LOC_Os10g11980	Acyl transferase	NS	Er to both RB and BB	NS	NS	Mori et al, 2007
2009	osssi2	Single recessive	LOC_Os01g69080	Fatty acid desaturase	NS	Er to both RB and BB	Retarded growth	Negatively regulates the defense responses partly through suppressing SA-responsive genes.	Jiang et al, 2009
2010	sl/spl1	Single recessive	LOC_Os12g16720	Cytochrome P450 monooxygenase CYP71P1.	ER	NS	NS	Catalyze the conversion of tryptamine to serotonin, mutant accumulate tryptamine.	Fujiwara et al, 2010
2010	rlin1/llm1	Single recessive	LOC_Os04g52130	Coproporphyrinogen III oxidase	NS	Er to BB	Similar to wild type	DR	Sun et al, 2011, Wang et al, 2015a
2012	oshpl3/cea62	Single recessive	LOC_Os02g02000	Hydroperoxide lyase (HPL), CYP74B2.	NS	Er to BB and SSB but more attractive to BPH.	DR	Affecting the levels of JA, GLVs and other volatiles, modulates rice-specific defense responses against different invaders.	Liu et al, 2012b, Tong et al, 2012
2014	spl29	Single recessive	LOC_Os08g10600	UDP-N-acetylglucosamine pyrophosphorylase 1	NS	Er to BB	Adversely impacted	Excessive accumulation of UDPG, JA and ABA.	Wang et al, 2015c, Xiao et al, 2018
2017	spl32	Single recessive	LOC_Os07g46460	Ferredoxin dependent glutamate synthase Fd-GOGAT)	In the chloroplasts	Er to BB	Adversely impacted	Decreased photorespiration rate and over-produced reactive oxygen species and damaged scavenging pathways.	Sun et al, 2017
2018	lmm9150	Single recessive	LOC_Os03g59610	Xanthoxin dehydrogenase, OsABA2.	NS	Er to both RB and BB	Enhanced growth but pre-harvest sprouting.	May resulted from altering of ABA biosynthesis, promoting JA signaling pathway.	Liao et al, 2018
2019	spl30-1	Single recessive	LOC_Os12g37870	ATP-citrate lyase ACL) A subunits.	NS	Er to BB	Adversely impacted	SPL30 is epistatic to OsSL in pathogen response pathway.	Ruan et al, 2018
2011	nls1-1D	Single semi-dominant	LOC_Os11g14380	CC-NB-LRR	NS	Er to BB	NS	NLS1 mediates both SA and NPR1-independent defense signaling pathways in rice.	Tang et al, 2011
2012	rls1	Single recessive	LOC_Os02g10900	NB-ARC domain containing protein	NS	NS	Rapid degradation of chlorophyll.	DR	Jiao et al, 2012
2016	dj-lm	Single recessive	LOC_Os09g39960	Dynamin-related protein, OsDRP1E.	Mitochondrial	Er to both RB and BB	NS	Affects the morphogenesis of cristae in mitochondria and causes the abnormal release of cytochrome c from mitochondria into cytoplasm.	Li et al, 2017

Year	Mutant/ gene name	Genetic mode	Gene ID	Protein encoded	Protein localization	Disease resistance	Effects on growth and development	Possible mechanisms involved	References
2002	spl7	Single recessive	LOC_Os05g45410	Heat stress transcription factor	NS	Er to RB.	NS	NS	Kojo et al, 2006, Yamanouchi et al, 2002
2005	oslsd1	Single recessive	LOC_Os08g06280	Zinc finger protein	Nucleus	Both RNAi and over expression conferred resistance against RB.	Overexpression accelerate callus differentiation, present dark green leaf color and promote seeds germination.	OsLOL1 interacted with OsbZIP58 to regulate the expression of the SOD1 and OsKO2 genes.	Wang et al, 2005
2005	NH1/OsNPR1	Single dominant	LOC_Os01g09800	BTB domain and ankyrin repeat region contained protein.	Cytosol and nucleus	Er to BB but susceptible to WBPH.	Similar to wild type.	Regulates the SA mediated resistance.	Chern et al, 2005, Yuan et al, 2007
2012	oslms	Single recessive	LOC_Os02g42600	Two double-stranded RNA binding motifs contain protein.	NS	Er to RB	Sensitive to cold stress.	NS	Undan et al, 2012
2009	spl5/ossl5	Single recessive	LOC_Os07g10390	A putative splicing factor 3b subunit 3 (SF3b3).	NS	Er to both RB and BB.	Adversely impacted.	Negative regulatory factor activating the serotonin metabolic pathway.	Chen et al, 2012, Jin et al, 2015, Ge et al, 2015
2016	lmm5	Two recessive	LOC_Os01g02720; LOC_Os04g50870	Eukaryotic translation elongation factor 1A (eEF1A)-like protein.	NS	Er to both RB and BB	NS	NS	Zhao et al, 2017
2016	spl33	Single recessive	LOC_Os01g02720	Eukaryotic translation elongation factor 1A (eEF1A)-like protein.	ER	Er to both RB and BB	NS	NS	Wang et al, 2017
2018	lml1/ spl^HM47	Single recessive	LOC_Os04g56480	Eukaryotic release factor 1 (eRF1).	ER and plasma membrane.	Er to both RB and BB.	Growth delay and smaller organs.	Forms a functional complex with SPL33/LMM5.1.	Qin et al, 2018, Zhang et al, 2018
2004	spl11	Single recessive	LOC_Os12g38210	U-box domain and an armadillo (ARM) repeat domain contained E3 ubiquitin ligase.	NS	Er to both RB and BB	Delayed flowering under long-day conditions.	SPL11 interacts with and mediated ubiquitination of SPIN6 to regulate OsRac1 associated defensome system; SPL11 also interacts with and ubiquitination SDS2 to regulate the RLCK118-OsRbohB mediated immunity. SPL11 negatively regulates SPIN1 to control flowering time.	Fan et al, 2018, Liu et al, 2012a, Liu et al, 2015, Vega-Sanchez et al, 2008, Zeng et al, 2004
2016	ebr1	Single recessive	LOC_Os05g19970	RING-type E3 ligase.	NS	Er to both RB and BB.	NS	EBR1 targets OsBAG4, a BAG protein promoting immunity and antimicrobial defense, to fine-tune immune homeostasis.	You et al, 2016
2017	oscul3a	Single recessive	LOC_Os02g51180	Cullin3-based RING E3 ubiquitin ligases (CRL3) component, CUL3a.	NS	Er to both RB and BB	NS	OsCUL3a interacts with and degrades OsNPR1.	Liu et al, 2017
2019	spl35	Single recessive	LOC_Os03g10750	CUE domain-containing protein.	Cytosol, ER and punctate compartment(s).	Er to both RB and BB	Adversely impacted	Involved in the mono-ubiquitination and vesicular trafficking pathways.	Ma et al, 2019
2011	spl3/osedr1/osacdr1	Single recessive	LOC_Os03g06410	Mitogen-Activated Protein Kinase Kinase Kinase	Nucleus	The osedr1 mutant possessed enhanced resistance to BB; OsAcdr1 over expression enhance RB resistance.	Delayed leaf senescence	OsEDR1 negatively regulates resistance via activation of ET biosynthesis; OsACDR1-OE plants accumulate phenolic compounds and secondary metabolites, and express enhanced levels of defense-related marker genes.	Wang et al, 2015b, Shen et al, 2011, Kim et al, 2009
2014	ospti1a/ttm1	Single recessive	LOC_Os05g04520	Protein kinase	Plasma membrane	Er to both RB and BB	Stunted growth	Regulates RAR1-dependent defense responses.	Matsui et al, 2015, Takahashi et al, 2007
2017	als1/lil1	Single semi-dominant	LOC_Os07g30510	Cysteine-rich receptor-like kinase (CRK).	Plasma membrane	Er to RB	NS	Activation of a common SA-, JA- and NH1-mediated defense response.	Du et al, 2019, Zhou et al, 2017
2018	sles	Single recessive	LOC_Os07g25680	Mitogen-Activated Protein Kinase Kinase Kinase	NS	Er to RB	Adversely impacted	NS	Lee et al, 2018
2019	psl	Single recessive	LOC_Os12g42420	Core 2/I branching beta-1,6-Nacetylglucosaminyl transferase	NS	NS	Adversely impacted	NS	Ke et al, 2019
2010	spl28	Single recessive	LOC_Os01g50770	Clathrin-associated adaptor protein complex 1, medium subunit μ1 (AP1M1)	Golgi	Er to both RB and BB	Adversely impacted.	Involved in post-Golgi trafficking pathway, accumulation of antimicrobial compounds.	Qiao et al, 2010
2015	lmr/lrd6-6/spl4	Single recessive	LOC_Os06g03940	AAA ATPase	Chloroplast, MVBs	Er to both RB and BB	Delayed leaf yellowing and adversely impacted.	Modulating MVBs-mediated vesicular trafficking and activating the biosynthesis of antimicrobial compounds.	Zhu et al, 2016, Song et al, 2018, Fekih et al, 2015
2015	rls2	Single recessive	LOC_Os04g58880	EXO70A1	Punctate signals both on the PM and within the nucleus	DR	NS	NS	Tu et al, 2015
2017	ossec3a	Single recessive	LOC_Os03g42750	Member of the exocyst complex, SEC3A.	Punctate distribution on the plasma membrane	Er to RB	Adversely impacted	OsSEC3A interacted with rice SNAP25-type t-SNARE protein OsSNAP32, which is involved in rice blast resistance.	Ma et al, 2018
2007	spl18	Single dominant	LOC_Os10g11980	Acyl transferase	NS	Er to both RB and BB	NS	NS	Mori et al, 2007
2009	osssi2	Single recessive	LOC_Os01g69080	Fatty acid desaturase	NS	Er to both RB and BB	Retarded growth	Negatively regulates the defense responses partly through suppressing SA-responsive genes.	Jiang et al, 2009
2010	sl/spl1	Single recessive	LOC_Os12g16720	Cytochrome P450 monooxygenase CYP71P1.	ER	NS	NS	Catalyze the conversion of tryptamine to serotonin, mutant accumulate tryptamine.	Fujiwara et al, 2010
2010	rlin1/llm1	Single recessive	LOC_Os04g52130	Coproporphyrinogen III oxidase	NS	Er to BB	Similar to wild type	DR	Sun et al, 2011, Wang et al, 2015a
2012	oshpl3/cea62	Single recessive	LOC_Os02g02000	Hydroperoxide lyase (HPL), CYP74B2.	NS	Er to BB and SSB but more attractive to BPH.	DR	Affecting the levels of JA, GLVs and other volatiles, modulates rice-specific defense responses against different invaders.	Liu et al, 2012b, Tong et al, 2012
2014	spl29	Single recessive	LOC_Os08g10600	UDP-N-acetylglucosamine pyrophosphorylase 1	NS	Er to BB	Adversely impacted	Excessive accumulation of UDPG, JA and ABA.	Wang et al, 2015c, Xiao et al, 2018
2017	spl32	Single recessive	LOC_Os07g46460	Ferredoxin dependent glutamate synthase Fd-GOGAT)	In the chloroplasts	Er to BB	Adversely impacted	Decreased photorespiration rate and over-produced reactive oxygen species and damaged scavenging pathways.	Sun et al, 2017
2018	lmm9150	Single recessive	LOC_Os03g59610	Xanthoxin dehydrogenase, OsABA2.	NS	Er to both RB and BB	Enhanced growth but pre-harvest sprouting.	May resulted from altering of ABA biosynthesis, promoting JA signaling pathway.	Liao et al, 2018
2019	spl30-1	Single recessive	LOC_Os12g37870	ATP-citrate lyase ACL) A subunits.	NS	Er to BB	Adversely impacted	SPL30 is epistatic to OsSL in pathogen response pathway.	Ruan et al, 2018
2011	nls1-1D	Single semi-dominant	LOC_Os11g14380	CC-NB-LRR	NS	Er to BB	NS	NLS1 mediates both SA and NPR1-independent defense signaling pathways in rice.	Tang et al, 2011
2012	rls1	Single recessive	LOC_Os02g10900	NB-ARC domain containing protein	NS	NS	Rapid degradation of chlorophyll.	DR	Jiao et al, 2012
2016	dj-lm	Single recessive	LOC_Os09g39960	Dynamin-related protein, OsDRP1E.	Mitochondrial	Er to both RB and BB	NS	Affects the morphogenesis of cristae in mitochondria and causes the abnormal release of cytochrome c from mitochondria into cytoplasm.	Li et al, 2017