Figure 2.

Drought tolerance genes that have been discovered or tested in model species and translated successfully into crop species. All of these genes have been expressed in engineered cereal crops and have been tested in field trials. Major agronomical traits, including yield, have been assessed, and conditions and drought performances have been successfully improved without negatively affecting plant growth or crop yield. (A) Hahb4: The sunflower transcription factor Hahb4 was expressed in soybean under the control of the native stress-inducible promoter of a homologous gene. Transgenic plants have reduced ethylene sensitivity, delayed senescence, increased osmoprotectant content, and an increased yield in the presence or absence of drought stress (Waltz, 2015). These plants are currently on the market as Verdeca Drought Tolerance Soybeans HB4^®. The same Hahb4 has also been transferred to bread wheat under the control of the constitutive promoter of maize ubiquitin 1 with similar promising results (Gonzalez et al., 2019; Ayala et al., 2019). (B) CspA, CspB: Maize plants overexpressing Escherichia coli CspB have high chlorophyll content, an improved photosynthetic rate, and reduced leaf area during vegetative growth. The best performing lines were commercialized as Genuity^® DroughtGard™ by Monsanto (now Bayer) in 2010 (Castiglioni et al., 2008; Nemali et al., 2015). (C) NF-YB1, NF-YB2: Maize plants overexpressing ZmNF-YB2 have higher stomatal conductance and chlorophyll content, and delayed senescence. These lines were not assessed in the field for performance under well-watered conditions and were never introduced to the market (Nelson et al., 2007). (D) TPS/TPP, TsVP: Carbon allocation, root/shoot ratio. In maize, floral-specific expression of T6P phosphatase (TPP) altered carbon allocation and improved yield in both well-watered and water-limited field trials (Nuccio et al., 2015). Also, in maize, the constitutive expression of the TsVP gene from the halophyte Thellungiella halophila under the control of the endogenous ubiquitin promoter increased total soluble sugars and proline under osmotic stress. Improvements in dehydration tolerance were assessed in a small-scale field trial (Li et al., 2008). (E) OsNACs, OsERF71, HVA1, DRO1. In rice, expression of the transcription factor OsNAC5 under the control of the root-specific promoter RCc3 improved drought and high salinity resistance by enlarging the root diameter. Yield improvements in normal and stress conditions were assessed in a 3-year field trial in three different locations (Jeong et al., 2013). Similar results were obtained with OsNAC9 and OsNAC10 (Jeong et al., 2010; Redillas et al., 2012). Root-specific expression. Also, in rice, the expression of the barley HVA1 under the control of a synthetic ABA-inducible promoter enhanced root growth, leading to better water use efficiency and abiotic stress tolerance. as confirmed by a small-scale field trial (Chen et al., 2015). The DRO1 allele from deep-rooting rice cultivars increases gravitropic response and root depth, increasing rice yield in both drought and normal conditions (Uga et al., 2013; Arai-Sanoh et al., 2014). (F) AtOSR1, ARGOS8: Arabidopsis ORGAN SIZE RELATED1 (AtOSR1) 1 and its maize homolog ZmARGOS1 improve dehydration avoidance in both plant species by reducing ethylene sensitivity (Shi et al., 2015); Moderate constitutive expression of ARGOS8, which was obtained by promoter swapping using clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) homology-directed recombination, improved drought tolerance in a field trial under stress conditions without affecting yield in well-watered control experiments (Shi et al., 2017). Commercialization of these lines is under evaluation by the developer Corteva Agriscience™ (former DuPont Pioneer).