OsPGIP1-Mediated Resistance to Bacterial Leaf Streak in Rice is Beyond Responsive to the Polygalacturonase of Xanthomonas oryzae pv. oryzicola

Abstract

Polygalacturonase-inhibiting proteins (PGIPs) have been shown to recognize fungal polygalacturonases (PGs), which initiate innate immunity in various plant species. Notably, the connection between rice OsPGIPs and PGs in Xanthomonas oryzae pv. oryzicola (Xoc), which causes bacterial leaf streak (BLS), remains unclear. Here, we show that OsPGIP1 was strongly induced after inoculating rice with the Xoc strain RS105. Furthermore, OsPGIP1-overexpressing (OV) and RNA interference (RNAi) rice lines increased and decreased, respectively, the resistance of rice to RS105, indicating that OsPGIP1 contributes to BLS resistance. Subsequently, we generated the unique PG mutant RS105Δpg, the virulence of which is attenuated compared to that of RS105. Surprisingly, the lesion lengths caused by RS105Δpg were similar to those caused by RS105 in the OV lines compared with wild-type ZH11 with reduced Xoc susceptibility. However, the lesion lengths caused by RS105Δpg were still significantly shorter in the OV lines than in ZH11, implying that OsPGIP1-mediated BLS resistance could respond to other virulence factors in addition to PGs. To explore the OsPGIP1-mediated resistance, RNA-seq analysis were performed and showed that many plant cell wall-associated genes and several MYB transcription factor genes were specifically expressed or more highly induced in the OV lines compared to ZH11 postinoculation with RS105. Consistent with the expression of the differentially expressed genes, the OV plants accumulated a higher content of jasmonic acid (JA) than ZH11 postinoculation with RS105, suggesting that the OsPGIP1-mediated resistance to BLS is mainly dependent on the plant cell wall-associated immunity and the JA signaling pathway.

Different Cell Wall-Degradation Ability Leads to Tissue-Specificity between Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola

“…However, no MR gene against Xoc is identified in rice until now [2], only some cell wall-related genes are associated with rice resistance to Xoc. The overexpression of polygalacturonase-inhibiting protein 1/4 (OsPGIP1/4) and small heat shock protein (OsHsp18.0-Cl) genes enhance resistance to bacterial leaf streak in rice [34][35][36]. The polygalacturonase-inhibiting protein functions in inhibiting the activity of enzymes which secreted by bacteria to degrade cell wall component-pectic polysaccharides [34].…”

Tal2c Activates the Expression of OsF3H04g to Promote Infection as a Redundant TALE of Tal2b in Xanthomonas oryzae pv. oryzicola

“…The Tal2c gene, including the 129 bp promoter and 3282 bp CDS, was amplified from HGA4 genomic DNA with special primers (Table S3) and then cloned into the pVSP61 vector to generate pVSP61-Tal2c. The pVSP61-Tal2c vector was transformed into RS105 competent cells according to previous studies [4,65]. The Xoc strains RS105, HGA4 and RS105/Tal2c were incubated on PSA plates for 2 to 3 days.…”

“…As previously reported [4], the 04gOE-1 was grown for 8 weeks along with ZH11, and leaves were collected for RNA extraction using a plant RNA kit (OMEGA Bio-Tek, Norcross, GA, USA). Three different repeats of RNA were used to construct libraries and perform RNA-seq by BGISEQ-500 (Beijing Genomics Institution, Shenzhen, China) according to previous reports [42,43,65]. The accession number (PRJNA781784) was obtained from the NCBI Sequence Read Archive (SRA) after submitting the raw sequence reads.…”

“…To construct the overexpression rice, the 1023 bp fragment of OsF3H 04g was amplified from ZH11 rice cDNA and cloned into the pCXUN-MYC vector to generate pUN-F3H04g. Gene editing of the rice genome was implemented by the CRISPR-Cas9 system according to previous reports [65,66]. The CRISPR-Cas9-mediated gene editing of gE-BETal2c (5 -TATTCCCTCGCGTGATC-3 ) in the OsF3H 04g promoter and gEBETal2b (5 -TCCGGCCCCTCTCCCCCCGCCACCTGAC-3 ) in the OsF3H 03g promoter was designed with the U3-gRNA targets 5 -GCCGGCCGGAGATCACGCGA-3 and 5 -AAGTCGAGTCAG GTGGCGGG-3 , respectively.…”

Recent Advances in Understanding the Function of the PGIP Gene and the Research of Its Proteins for the Disease Resistance of Plants

“…A recent study on rice showed that the PGIP4-containing chromosome is related to the resistance of bacterial stripe disease, with increased susceptibility to bacterial stripe disease in rice when the PGIP4 is silenced by RNAi [78]. RNA-seq analysis revealed that the OsPGIP1-mediated resistance of bacterial leaf streak is induced by PG of Xoc and other pathogenicity factors, and is primed by the activated expression of PR genes, cell wall defense-associated genes and regulators, and an accumulation of JA [85]. Increased PGIP in potato improved the resistance of Ralstonia solanacearum [86].…”