Transgenic insertion of the cyanobacterial membrane protein ictB increases grain yield in Zea mays through increased photosynthesis and carbohydrate production

PLoS One. 2021 Feb 4;16(2):e0246359. doi: 10.1371/journal.pone.0246359. eCollection 2021.

Abstract

The C4 crop maize (Zea mays) is the most widely grown cereal crop worldwide and is an essential feedstock for food and bioenergy. Improving maize yield is important to achieve food security and agricultural sustainability in the 21st century. One potential means to improve crop productivity is to enhance photosynthesis. ictB, a membrane protein that is highly conserved across cyanobacteria, has been shown to improve photosynthesis, and often biomass, when introduced into diverse C3 plant species. Here, ictB from Synechococcus sp. strain PCC 7942 was inserted into maize using Agrobacterium-mediated transformation. In three controlled-environment experiments, ictB insertion increased leaf starch and sucrose content by up to 25% relative to controls. Experimental field trials in four growing seasons, spanning the Midwestern United States (Summers 2018 & 2019) and Argentina (Winter 2018 & 2019), showed an average of 3.49% grain yield improvement, by as much as 5.4% in a given season and up to 9.4% at certain trial locations. A subset of field trial locations was used to test for modification of ear traits and ФPSII, a proxy for photosynthesis. Results suggested that yield gain in transgenics could be associated with increased ФPSII, and the production of longer, thinner ears with more kernels. ictB localized primarily to the microsome fraction of leaf bundle-sheath cells, but not to chloroplasts. Extramembrane domains of ictB interacted in vitro with proteins involved in photosynthesis and carbohydrate metabolism. To our knowledge, this is the first published evidence of ictB insertion into a species using C4 photosynthesis and the largest-scale demonstration of grain yield enhancement from ictB insertion in planta. Results show that ictB is a valuable yield gene in the economically important crop maize, and are an important proof of concept that transgenic manipulation of photosynthesis can be used to create economically viable crop improvement traits.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Argentina
  • Biomass
  • Carbohydrate Metabolism / genetics
  • Carbohydrates / biosynthesis
  • Carbohydrates / genetics
  • Carbon Cycle
  • Carbon Dioxide / metabolism
  • Chlorophyll / metabolism
  • Chloroplasts / metabolism
  • Crop Production
  • Cyanobacteria / genetics
  • Cyanobacteria / metabolism*
  • Membrane Proteins / genetics
  • Midwestern United States
  • Photosynthesis / genetics*
  • Plant Leaves / metabolism
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • Zea mays / genetics
  • Zea mays / growth & development
  • Zea mays / metabolism*

Substances

  • Carbohydrates
  • Membrane Proteins
  • Chlorophyll
  • Carbon Dioxide

Grant support

This work was funded by Benson Hill (https://bensonhill.com/), a for-profit agricultural technology company, as part of its research and development program. Benson Hill provided all funding for the study, including study design, data collection and analysis, manuscript preparation, publication, and salaries for all of the authors.