The MYB transcription factor OsMYBxoc1 regulates resistance to Xoc by directly repressing transcription of the iron transport gene OsNRAMP5 in rice

Haimiao Zhang; Baolong Sun; Wei Wu; Yang Li; Ziyi Yin; Chongchong Lu; Haipeng Zhao; Lingguang Kong; Xinhua Ding

doi:10.1016/j.xplc.2024.100859

The MYB transcription factor OsMYBxoc1 regulates resistance to Xoc by directly repressing transcription of the iron transport gene OsNRAMP5 in rice

Plant Commun. 2024 Mar 5:100859. doi: 10.1016/j.xplc.2024.100859. Online ahead of print.

Authors

Haimiao Zhang¹, Baolong Sun¹, Wei Wu¹, Yang Li¹, Ziyi Yin¹, Chongchong Lu¹, Haipeng Zhao¹, Lingguang Kong¹, Xinhua Ding²

Affiliations

¹ State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, College of Plant Protection, Shandong Agricultural University, Tai'an 271018, China.
² State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, College of Plant Protection, Shandong Agricultural University, Tai'an 271018, China. Electronic address: xhding@sdau.edu.cn.

PMID: 38444161
DOI: 10.1016/j.xplc.2024.100859

Abstract

Bacterial leaf streak caused by Xanthomonas oryzae pv. oryzicola (Xoc) is a continuous threat to rice cultivation, leading to substantial yield losses with socioeconomic implications. Iron ions are essential mineral nutrients for plant growth, but little information is available on how they influence mechanisms of rice immunity against Xoc. Here, we investigated the role of the myeloblastosis-related (MYB) transcriptional repressor OsMYBxoc1 in modulation of rice resistance through control of iron ion transport. Overexpression of OsMYBxoc1 significantly increased rice resistance, whereas OsMYBxoc1 RNA-interference lines and knockout mutants showed the opposite result. Suppression of OsMYBxoc1 expression dampened the immune response induced by pathogen-associated molecular patterns. We demonstrated that OsMYBxoc1 binds specifically to the OsNRAMP5 promoter and represses transcription of OsNRAMP5. OsNRAMP5, a negative regulator of rice resistance to bacterial leaf streak, possesses metal ion transport activity, and inhibition of OsMYBxoc1 expression increased the iron ion content in rice. Activity of the ion-dependent H₂O₂ scavenging enzyme catalase was increased in plants with suppressed expression of OsMYBxoc1 or overexpression of OsNRAMP5. We found that iron ions promoted Xoc infection and interfered with the production of reactive oxygen species induced by Xoc. The type III effector XopAK directly inhibited OsMYBxoc1 transcription, indicating that the pathogen may promote its own proliferation by relieving restriction of iron ion transport in plants. In addition, iron complemented the pathogenicity defects of the RS105_ΔXopAK mutant strain, further confirming that iron utilization by Xoc may be dependent upon XopAK. In conclusion, our study reveals a novel mechanism by which OsMYBxoc1 modulates rice resistance by regulating iron accumulation and demonstrates that Xoc can accumulate iron ions by secreting the effector XopAK to promote its own infection.

Keywords: bacterial leaf streak; effector; metal ion; pathogen; plant immunity.