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. 2022 Mar 10;13:850588. doi: 10.3389/fmicb.2022.850588

Table 2.

The mechanisms of Citrus Huanglongbing (HLB)-tolerant citrus elucidated by multi-omics approaches.

Citrus genotypes Putative tolerance mechanisms of citrus to HLB References
Poncirus trifoliata and hybrids Constitutive disease resistance 1 (CDR1) genes activate PR1 expression
Downregulation of gibberellin (GA) synthesis and the induction of cell wall strengthening
Poncirus trifoliata hybrids (US-942) have a stronger defense response, more efficient nutrient uptake and increased accumulation of secondary metabolites, flavonoids, phenolics, and volatile organic compounds (VOC).
Increased accumulation of phenylalanine, tyrosine, and tryptophan, and some sugars such as mannose, and α-D-mannopyranoside which are important in secondary metabolite biosynthesis and reduction of availability of essential sugars for Candidatus Liberibacter asiaticus (CLas) survival
Folimonova et al., 2009; Albrecht and Bowman, 2011, 2012; Killiny and Hijaz, 2016; Killiny, 2017; Curtolo et al., 2020; Huang et al., 2021b
Ichang papeda (Citrus ichangensis “2586”) Carbohydrate metabolism, photosynthesis process, and amino acids are not activated during CLas infection, which may suppress HLB development
Upregulation of genes involved in secondary metabolism, such as the isoprenoid and flavonoid biosynthesis pathways
Wu et al., 2020
“Jackson” grapefruit (Citrus paradisi Macf) Increased expression of NPR1-like genes and secondary metabolite pathways Wang et al., 2016
Mexican lime (Citrus aurantifolia) Increase expression of genes related to cell wall, secondary metabolism, transcription factors, signaling, and redox reactions Arce-Leal et al., 2020
Rough lemon (Citrus jambhiri) Upregulation of genes involved in maintaining or recovering of phloem transport activity and possible enhancement of stress tolerance Fan et al., 2012
Kaffir lime (Citrus hystrix) Upregulation of genes involved in cell wall metabolism and secondary metabolism
Increased expression of peroxidases, Cu/Zn-SOD, and POD4 genes
Zou et al., 2019
Sydney hybrid (Microcitrus virgata) Strong defense response upon CLas infection, more efficient nutrient uptake and increased accumulation of secondary metabolites, flavonoids, phenolics, and VOC Huang et al., 2021a,b
Australian finger lime (Microcitrus australiasica) Production of stable antimicrobial peptides, induction of defense responses such as salicylic acid (SA) biosynthesis, phenylpropanoid pathways, and defense genes Huang et al., 2021a
Volkamer lemon (Citrus Volkameriana) Upregulation of four glutathione-S-transferases proteins involved in radical ion detoxification Martinelli et al., 2016
Lisbon lemon (Citrus limon) Upregulation of genes involved in defense responses Ramsey et al., 2020
Curry leaf [Murraya koenigii (L.) Spreng] High level of phenolics and flavonoids with antimicrobial activity Killiny et al., 2017; Hijaz et al., 2020
LB8-9 Sugar Belle {“Clementine” mandarin (Citrus reticulata) × “Minneola” tangelo [(Citrus x Tangelo), “Duncan” grapefruit (Citrus paradisi) × “Dancy” tangerine (C. reticulata)]} Increased accumulation of phenolics, flavonoids, and VOCs with known antimicrobial activity such as aldehydes, monoterpenes, and sesquiterpenes
Increase accumulation of plant hormones responsible for plant growth and phloem regeneration
Killiny et al., 2017; Deng et al., 2021; Suh et al., 2021