TAL effector driven induction of a SWEET gene confers susceptibility to bacterial blight of cotton

Authors: COX, KEVIN - Texas A&M University; MENG, FANHONG - Texas A&M University; WILKINS, KATHERINE - Cornell University; LI, FANGJUN - Texas A&M University; WANG, PING - Texas A&M University; BOOHER, NICHOLAS - Cornell University; CARPENTER, SARA - Cornell University; CHEN, LI-QING - University Of Illinois; ZHENG, HUI - Cornell University; GAO, XIQUAN - Texas A&M University; ZHENG, YI - Cornell University; FEI, ZHANGJUN - Cornell University; Yu, John; ISAKEIT, THOMAS - Texas A&M University; WHEELER, TERRY - Texas A&M University; FROMMER, WOLF - Texas A&M University; HE, PING - Texas A&M University; BOGDANOVE, ADAM - Cornell University; SHAN, LIBO - Texas A&M University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2017
Publication Date: 5/24/2017
Citation: Cox, K.L., Meng, F., Wilkins, K.E., Li, F., Wang, P., Booher, N.J., Carpenter, S., Chen, L., Zheng, H., Gao, X., Zheng, Y., Fei, Z., Yu, J., Isakeit, T., Wheeler, T., Frommer, W.B., He, P., Bogdanove, A.J., Shan, L. 2017. TAL effector driven induction of a SWEET gene confers susceptibility to bacterial blight of cotton. Nature Communications. 8:15588.

Interpretive Summary: Bacterial blight is one of the most destructive diseases in cotton and it causes a very significant yield loss to cotton production. Genetic manipulation of resistance or susceptibility to the disease in the crop plant is one of the most effective approaches to protecting the crop production from its yield loss. Currently, however, our understanding of the molecular mechanism of host-pathogen interactions is limited in cotton bacterial blight. No resistant or susceptible genes for the disease have yet been cloned or molecularly identified, primarily due to the large and complex polyploid cotton genome. In this study, we sequenced two disease-causing bacterial strain genomes (accessions H1005 and N1003) and then analyzed all transcription activator-like (TAL) effector genes in the bacterial genomes. With the recently published Upland cotton genome (accession TM-1), we molecularly identified a cotton gene named GhSWEET10 that is specifically induced by a bacterial avirulence gene named Avrb6. We then discovered that the induction of this gene and additional GhSWEET genes was substantially reduced in bacterial blight resistant cotton carrying the recessive b6 resistance gene. Identification of sugar-transporting GhSWEETs as major bacterial blight susceptibility genes and a novel resistance mechanism to the disease represents an important advance in molecular understanding of bacterial blight and its resistance in cotton. The new knowledge will facilitate the strategic development of durable, broad-spectrum resistance to the disease in cotton production.

Technical Abstract: Bacterial blight of cotton (BBC), caused by Xanthomonas citri subsp. malvacearum (Xcm), is among the most destructive diseases in cotton (Gossypium spp.). Transcription activator-like (TAL) effectors from Xcm are essential for BBC disease progression. Here, we carried out whole-genome PacBio-sequencing and assembled the full repertoires of TAL effectors of two well-studied Xcm strains, H1005 and N1003. By combining genome-wide transcriptome profiling with TAL effector binding element (EBE) computational prediction, we discovered that cotton GhSWEET10, encoding a clade III functional SWEET sucrose transporter, is specifically induced by Avrb6, a key TAL effector determining the pathogenicity in XcmH1005, via the EBE of the GhSWEET10 promoter. Activation of GhSWEET10 by designer TAL effectors restored virulence to Xcm avrb6 deletion strains, and virus-induced gene silencing (VIGS) of GhSWEET10 compromised susceptibility to infection by Xcm carrying avrb6. Intriguingly, despite of bearing a same EBE, a BBC-resistant cotton line carrying the recessive b6 resistance gene showed largely reduced Avrb6-mediated induction of GhSWEET10, suggesting a novel mechanism involved in BBC resistance. Extensive survey of the transcriptional responsiveness of GhSWEETs to a wide range of Xcm field isolates revealed the involvement of additional GhSWEETs in BBC and likely fast acquisition of TAL effectors in Xcm. Identification of GhSWEETs as important BBC susceptibility genes represents an important advance in molecular understanding of the disease and resistance in cotton with a complex and polyploid genome, and facilitates the strategic development of durable resistance to BBC.