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Title: Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for Citrus Huanglongbing Disease

Author
item ZHAO, HONGWEI - University Of California
item SUN, RUOBAI - University Of California
item Albrecht, Ute
item PADMANABHAN, CHELLAPPAN - University Of California
item WANG, AIRONG - University Of California
item COFFEY, MICHAEL - University Of California
item GIRKE, THOMAS - University Of California
item WANG, ZONGHUA - Fuijan Agricultural University
item CLOSE, TIMOTHY - University Of California
item ROOSE, MIKEAL - University Of California
item Yokomi, Raymond - Ray
item FOLIMONOVA, SVETLANA - University Of Florida
item VIDALAKIS, GEORGIOS - University Of California
item ROUSE, ROBERT - University Of Florida
item Bowman, Kim
item JIN, HAILING - University Of California

Submitted to: Molecular Plant
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/21/2012
Publication Date: 2/19/2013
Citation: Zhao, H., Sun, R., Albrecht, U., Padmanabhan, C., Wang, A., Coffey, M.D., Girke, T., Wang, Z., Close, T.J., Roose, M., Yokomi, R.K., Folimonova, S., Vidalakis, G., Rouse, R., Bowman, K.D., Jin, H. 2013. Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for Citrus Huanglongbing Disease. Molecular Plant. 6(2):301-310.

Interpretive Summary: Huanglongbing (HLB) is a devastating disease of citrus that is associated with the bacteria Candidatus Liberibacter asiaticus (Las). A study was conducted to identify small host Ribonucleic acid (RNAs)that are associated with Las infection and HLB disease development. Many small RNAs were identified that were induced or reduced following Las infection, some of which may be useful for diagnostics and more detailed studies of the disease and its effects on the host. It was demonstrated that one of these small RNAs, miR399, was not induced by another disease of citrus, citrus stubborn, that has similar symptoms to HLB. MiR399 had been previously shown to be associated with phosphorus starvation in other plant species. The small RNA appeared specfic for development of HLB disease, and also indicated an association between phosphorus deficiency and the disease. A nutritional analysis confirmed that Las-infected citrus trees had reduced phosphorus content. A field study demonstrated that application of additional phosphorus to field-grown HLB-positive citrus trees reduced HLB symptoms. The molecular, physiological and field results suggest that phosphorus deficiency is linked to HLB disease symptomology.

Technical Abstract: Huanglongbing (HLB) is a devastating citrus disease that is associated with bacteria of the genus Candidatus Liberibacter(Ca. L.). Powerful diagnostic tools and management strategies are desired to control HLB. Host small Ribonucleic acid (sRNA) play a vital role in regulating host responses to pathogen infection and are used as early diagnosis markers for many human diseases, including cancers. To determine whether citrus sRNAs regulate host responses to HLB, sRNAs were profiled from Citrus sinensis 10- and 14-week post grafting with Ca. L. asiaticus (Las)-positive or healthy tissue. Ten new microRNAs (miRNAs), 76 conserved miRNAs and many small interfering RNAs (siRNAs) were discovered. Several miRNAs and siRNAs were highly induced by Las infection, which can be potentially developed into early diagnosis markers of HLB. MiR399 was induced specifically by infection of Las but not Spiroplasma citri, the causal agent of citrus stubborn, a disease with symptoms similar to HLB. Because miR399 is induced by phosphorus starvation in other plant species, we examined the phosphorus content and found a 35% reduction in Las-positive citrus trees compared to healthy trees. Applying phosphorus oxyanion solutions to HLB-positive ‘Hamlin’ sweet orange trees reduced HLB symptom severity during a 3-year field trial in southwest Florida. Phosphorus is an essential element for DNA, RNA, phosphoproteins, and energy-rich phosphate compounds, and is involved in many cellular processes, including photosynthesis and energy reactions. Our molecular, physiological and field data suggest that phosphorus deficiency is linked to HLB disease symptomology.