The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube

Lixin Wang; Shiyan Liu; Mengjiao Gao; Lihu Wang; Linxia Wang; Yunjie Wang; Li Dai; Jin Zhao; Mengjun Liu; Zhiguo Liu

doi:10.3389/fmicb.2022.800762

The Crosstalk of the Salicylic Acid and Jasmonic Acid Signaling Pathways Contributed to Different Resistance to Phytoplasma Infection Between the Two Genotypes in Chinese Jujube

Front Microbiol. 2022 Mar 18:13:800762. doi: 10.3389/fmicb.2022.800762. eCollection 2022.

Authors

Lixin Wang^{1

2}, Shiyan Liu¹, Mengjiao Gao¹, Lihu Wang³, Linxia Wang¹, Yunjie Wang¹, Li Dai^{1

2}, Jin Zhao⁴, Mengjun Liu^{1

2}, Zhiguo Liu^{1

2}

Affiliations

¹ College of Horticulture, Hebei Agricultural University, Baoding, China.
² Research Center of Chinese Jujube, Hebei Agricultural University, Baoding, China.
³ School of Landscape and Ecological Engineering, Hebei University of Engineering, Handan, China.
⁴ College of Life Science, Hebei Agricultural University, Baoding, China.

Abstract

Jujube witches' broom disease (JWB), one of the most serious phytoplasma diseases, usually results in the destruction of Chinese jujube (Ziziphus jujuba Mill.). Although most jujube cultivars are sensitive to JWB, we found a few genotypes that are highly resistant to JWB. However, the molecular mechanism of phytoplasma resistance has seldom been studied. Here, we used Chinese jujube "T13," which has strong resistance to JWB, and a typical susceptible cultivar, "Pozao" ("PZ"), as materials to perform comparative transcriptome, hormone, and regulation analyses. After phytoplasma infection, the differential expression genes (DEGs) were detected at all three growth phases (S1, S2, and S3) in "PZ," but DEGs were detected only at the first growth phase in "T13." Meanwhile, no phytoplasma was detected, and the symptoms especially witches' broom caused by JWB were not observed at the last two growth phases (S2 and S3) in "T13." Protein-protein interaction analysis also showed that the key genes were mainly involved in hormone and reactive oxygen species (ROS) signaling. In addition, during the recovered growth phase in "T13" from S1 to S2, the level of hydrogen peroxide (H₂O₂) was significantly increased and then decreased from S2 to S3. Moreover, jasmonic acid (JA) was significantly accumulated in "PZ" diseased plants, especially at the S2 phase and at the S2 phase in "T13," while the content of salicylic acid (SA) decreased significantly at the S2 phase of "T13" compared to that in "PZ." The changes in H₂O₂ and JA or SA were consistent with the changes in their key synthesis genes in the transcriptome data. Finally, exogenous application of an SA inhibitor [1-aminobenzotriazole (ABT)] rescued witches' broom symptoms, while the contents of both JA and MeJA increased after ABT treatment compared to the control, demonstrating that exogenous application of an SA inhibitor rescued the symptoms of jujube after phytoplasma infection by decreasing the contents of SA and increasing the contents of JA and MeJA. Collectively, our study provides a new perspective on the transcriptional changes of Chinese jujube in response to JWB and novel insights that the crosstalk of JA and SA signaling communicated together to contribute to "T13" JWB resistance.

Keywords: Chinese jujube; ROS; jasmonic acid; phytoplasma; salicylic acid; signaling.