Abstract
Transgenic maize (Zea mays) that expresses rice (Oryza sativa) TREHALOSE PHOSPHATE PHOSPHATASE1 (TPP1) from the rice MADS6 promoter, which is active over the flowering period, produces higher yields than wild type. This yield increase occurs with or without drought conditions during flowering. To understand the mechanistic basis of the increased yield, we characterized gene expression and metabolite profiles in leaves and developing female reproductive tissue, comprising florets, node, pith, and shank, over the flowering period with and without drought. The MADS6 promoter was most active in the vasculature, particularly phloem companion cells in florets and pith, consistent with the largest decreases in trehalose 6-phosphate (T6P) levels (2- to 3-fold) being found in pith and florets. Low T6P led to decreased gene expression for primary metabolism and increased gene expression for secondary metabolism, particularly lipid-related pathways. Despite similar changes in gene expression, the pith and floret displayed opposing assimilate profiles: sugars, sugar phosphates, amino acids, and lipids increased in florets, but decreased in pith. Possibly explaining this assimilate distribution, seven SWEET genes were found to be up-regulated in the transgenic plants. SnRK1 activity and the expression of the gene for the SnRK1 beta subunit, expression of SnRK1 marker genes, and endogenous trehalose pathway genes were also altered. Furthermore, leaves of the transgenic maize maintained a higher photosynthetic rate for a longer period compared to wild type. In conclusion, we found that decreasing T6P in reproductive tissues down-regulates primary metabolism and up-regulates secondary metabolism, resulting in different metabolite profiles in component tissues. Our data implicate T6P/ SnRK1 as a major regulator of whole-plant resource allocation for crop yield improvement.
Highlights
Leaf gas exchange measurements of well-watered and water-stressed maize plants were carried out using a portable infra-red open gas exchange system (LI6400XT; LI-COR) under the growing conditions, leaf temperature 27°C, photosynthetic photon flux density 600 mmol m–2 s–1, and relative air humidity 65 6 5%
Two independent transgenic lines (5217 and 5224) of maize (Zea mays) expressing the OSMADS6: TPP1 construct, wild-type line A188, and OSMADS6: GUS were grown in a controlled environment (600 mmol m22 s21, 16 h day, 80/70% relative humidity day/night, 27°C/21°C day/night in Rothamsted compost supplemented with full nutrition as in Nuccio et al, 2015)
Five biological replicates from individual plants were taken for each line, time, and tissue
Summary
Two independent transgenic lines (5217 and 5224) of maize (Zea mays) expressing the OSMADS6: TPP1 construct, wild-type line A188, and OSMADS6: GUS were grown in a controlled environment (600 mmol m22 s21, 16 h day, 80/70% relative humidity day/night, 27°C/21°C day/night in Rothamsted compost supplemented with full nutrition as in Nuccio et al, 2015). Five biological replicates from individual plants were taken for each line, time, and tissue. Plants were grown under full irrigation, or with drought imposed 5 d before the first sampling point by withholding water until pots reached 65% of the weight before withholding water, as in Nuccio et al (2015). This level of drought was maintained throughout the sampling period by weighing plants daily. OSMADS6: GUS expression cassette activity was assessed by histochemical localization of GUS protein (described in Nuccio et al, 2015)
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