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Title: Accumulation of high OPDA level correlates with reduced ROS and elevated GSH benefiting white cell survival in variegated leaves

Author
item SUN, YING-HSUAN - Chung Hsing University
item HUNG, CHIU-YUEH - North Carolina State University
item QIU, JIE - Zheijiang University
item CHEN, JIANJUN - University Of Florida
item KITTUR, FAROOQAHMED - North Carolina State University
item OLDHAM, CARLA - North Carolina State University
item HENNY, RICHARD - University Of Florida
item Burkey, Kent
item FAN, LONGIJIANG - Zheijiang University
item XIE, JIAHUA - North Carolina State University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/2/2017
Publication Date: 3/9/2017
Citation: Sun, Y., Hung, C., Qiu, J., Chen, J., Kittur, F., Oldham, C., Henny, R., Burkey, K.O., Fan, L., Xie, J. 2017. Accumulation of high OPDA level correlates with reduced ROS and elevated GSH benefiting white cell survival in variegated leaves. Scientific Reports. 7:44158.

Interpretive Summary: Photosynthesis in higher plants occurs in special organelles called chloroplasts present in leaves and other green tissues. Formation of chloroplasts requires the expression of genes from both the cell nucleus and the organelle itself. The complexity of this process is illustrated in naturally variegated plants that develop leaves containing both green tissue with normal chloroplasts and either white or yellow tissue where chloroplast development is arrested at an early stage due to down regulation of pigment synthesis. The absence of chlorophyll causes a distinctly different form of leaf physiology in the white and yellow tissue types. In this study, 12-oxo phytodienoic acid (OPDA), a phytohormone, was found to be elevated 9-fold in white leaf tissue of the variegated house plant Epipremnum aureum ‘Marble Queen’. Elevated OPDA was shown to alter the expression of several different types of stress tolerance genes. The results suggest that OPDA plays a critical role in maintaining the viability of white sector leaf cells by reprogramming gene expression to accommodate the unusual physiology. These findings help lay the groundwork for future research on manipulating chloroplasts to facilitate the manufacture of biopharmaceuticals.

Technical Abstract: Variegated Epipremnum aureum ‘Marble Queen’ plant has white (VMW) and green (VMG) sectors within the same leaf. The white sector cells containing undifferentiated chloroplasts are viable, but the underlying mechanism for their survival is not clear. Because phytohormones are important for plant growth and development, those with their precursors produced in chloroplasts were compared and only 12-oxo phytodienoic acid (OPDA) was 9-fold higher in VMW than VMG. To reveal the consequences related to elevated OPDA, transcriptome profiles between VMW and VMG were compared. A total of 850 differentially expressed genes (DEGs) (FDR<0.05) were identified with 566 annotated. Compared to VMG, 21.5% of up- and 11% of down-regulated DEGs in VMW were involved in modulating transcription activities in which approximately 70% are stress-related transcription factors, indicating that a major transcriptome reprogramming occurred to deal with stress. About 5% of each annotated DEGs for ROS scavengers, DNA replication and repair, as well as protein chaperones were up-regulated uniquely in VMW. We verified OPDA-responsive DEGs in OPDA-treated green plants, which could potentially protect DNAs and proteins from oxidative damage and reduce ROS levels as demonstrated. OPDA has been implicated as a signal molecule to induce a group of genes through increasing glutathione (GSH) to alter the redox state of the cells for stress tolerance. We also observed higher levels of GSH in VMW which correlates well with the action mode of OPDA. Our results reveal a unique strategy employed by white cells to survive in VMW sectors.