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Title: Maize w3 disrupts homogentisate solanesyl transferase (ZmHst) and reveals a plastoquinone-9 independent path for phytoene desaturation and tocopherol accumulation in kernels

item Hunter, Charles
item SAUNDERS, JONATHAN - University Of Florida
item MAGALLANES-LUNDBACK, MARIA - Michigan State University
item Christensen, Shawn
item Willett, Denis
item Stinard, Philip
item Li, Qin-Bao
item LEE, KWANGHEE - University Of Connecticut
item DELLAPENNA, DEAN - Michigan State University
item KOCH, KAREN - University Of Florida

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/12/2017
Publication Date: 1/8/2018
Citation: Hunter III, C.T., Saunders, J., Magallanes-Lundback, M., Christensen, S.A., Willett, D.S., Stinard, P.S., Li, Q., Lee, K., Dellapenna, D., Koch, K.E. 2018. Maize w3 disrupts homogentisate solanesyl transferase (ZmHst) and reveals a plastoquinone-9 independent path for phytoene desaturation and tocopherol accumulation in kernels. Plant Journal. doi:10.1111/tpj.13821.

Interpretive Summary: Complex networks of hormones, pigments, and secondary metabolites govern the ability of crops to protect themselves against unfavorable growing conditions. Exposure to environmental stresses and biotic attacks result in billions of dollars in crop loss annually for corn growers alone. This work by scientists in the Chemistry Research Unit at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL contributes three key findings towards our understanding the regulatory dynamics surrounding a plant’s response to stress, and in doing so furthers our ultimate goal of improving crop resiliency and protecting against loss. First, we have revealed the molecular basis for a classic maize mutant, white seedling 3 (w3), which has been used as a model for carotenoid (a plant pigment and vitamin A precursor) deficiency in numerous studies since its discovery in 1923. We show that w3 mutants are disrupted in an enzyme responsible for plastoquinone (PQ) biosynthesis, thus explaining the carotenoid-deficiency, albino seedlings, and early-germinating seeds of w3 mutants. Our second major contribution resulted from our examination of plant chemical compounds, which revealed that w3 mutants unexpectedly produce a small amount of carotenoids and other downstream products, including an important plant hormone, ABA. This finding shows that our previous understanding of PQ’s role in the production of compounds important for plant defense and environmental stress was oversimplified, and that other compounds besides PQ may play a role in the production of carotenoids and ABA. Finally, our work here implicates PQ and its products in protecting vitamin E compounds, including a nutritionally-important, grain-specific species of vitamin E. Together, these findings improve our understanding of the regulation of a complex network of pigments, hormones, and vitamins that occur in plants. Besides being applied to helping us improve the ability of crops to withstand changing climates and attacks by pathogens, this knowledge may enable future work aimed at improving the nutritional quality of maize and other grains.

Technical Abstract: Maize white seedling 3 (w3) has been used to study carotenoid deficiency for almost 100 years, although its genetic basis remained unknown. We show here that w3 phenotype is caused by disruption of homogentisate solanesyl transferase (HST), which catalyzes the first committed step in plastoquinone-9 (PQ9) biosynthesis. The resulting PQ9 deficiency, in turn, contributes to the w3 phenotype through defects in at least three key functions of PQ9: 1) as a redox cofactor for electron and proton transfer during photosynthesis, 2) as an oxidant in the enzymatic desaturation of phytoene during formation of carotenoids, and 3) as the immediate precursor for plastochromanol-8, a vitamin E that functions as a lipid-soluble antioxidant. Accordingly, w3 seedlings are albino, lack carotenoids, and accumulate phytoene. However, despite lacking detectable levels of the PQ9 cofactor for phytoene desaturation, w3 seedlings can produce abscisic acid (ABA) in darkness, and kernels accumulate sufficient levels to support seed maturation. The presence of ABA in w3 nulls indicates that although carotenoids were near limits of detection, minimal flux through this biosynthetic pathway can allow ABA accumulation in the absence of measurable PQ9. Phytoene desaturase may thus be able to use, albeit inefficiently, an alternate oxidant cofactor. We also tested the hypothesis that indirect effects of PQ9 deficiency on tocochromanol accumulation would be minimal in the non-photosynthetic maize grain. Tocopherol decreases in w3 kernels were generally small and varied with genetic background, and the tocotrienols distinctive to grain species were essentially unaffected. In addition to identifying the basis for the long-enigmatic w3 maize mutant, we show that PQ9-independent phytoene desaturation can occur in w3 seedlings and demonstrate that PQ9 and carotenoid have minimal impact on vitamin E species of non-potosynthetic maize grains.