Sketch of the hypothetical pathway of HLB-tolerant and HLB-susceptible citrus species in response to CLas.

In HLB-tolerant citrus species, first, CLas invasion causes cell signaling, which enhances the secondary metabolic genes [160] to biosynthesize antimicrobial compounds such as volatiles, fatty acids, amino acids, and some antibacterial compounds such as flavonol, flavone, and flavanone [124]; second, CLas may secrete PAMPs and pathogen virulence factors into the phloem to interfere with various targets [7] such as genes, proteins, and metabolites. In HLB-tolerant citrus, the MAPK [133] activates the downstream defense-related genes such as WRKY genes to trigger the PR reaction and strongly induce SA-mediated defense response [168], and the expression of DIR1 genes, NPR4, SA-related genes will be induced to contribute to the high HLB tolerance [143]. In HLB-susceptible citrus species, first, CLas infection affects the photosynthesis and primary metabolism, decreases starch degradation enzymes, increases the expression of starch biosynthetic genes (such as GBSS1 and glgC), and induces PP2 gene, which triggers starch and callose accumulation and causes phloem plugging [118]. Disruption of primary metabolism causes delayed or reduced biosynthesis of secondary metabolites (antibacterial compounds such as flavonols), and susceptible citrus shows severe symptoms; second, the CLas secretes virulence factor proteins such as a functional enzyme SahA into citrus plant, destroying the host’s SA and its derivatives to suppress the host defense [116]. In addition, SDEs move into cells via the Sec-dependent secretion system; SDEs such as SDE1 interact with receptor protein PLCP and suppress its activity, which weakens the citrus plant defense response [107]. Moreover, the SDE15 interacts with citrus protein CsACD2 and suppresses the plant immunity and promotes CLas multiplication [110]. In this way, the CLas protein disrupts the normal metabolism and defense system of host cells by modifying the host cellular machinery to manipulate pathogenicity and to make the host environment favorable for CLas survival and progression. ACP, Asian citrus psyllid; HLB, Huanglongbing; MAPK, mitogen-activated protein kinase; PAMP, pathogen-associated molecular pattern; PLCP, papain-like cysteine protease; PR, pathogen-related; SA, salicylic acid; SahA, salicylate hydroxylase; SDE, Sec-delivered effector.