Green Revolution DELLAs: From translational reinitiation to future sustainable agriculture

The Green Revolution (GR) of the 1960s saw spectacular increases in cereal crop yields, enabled by widespread adoption high-yielding semi-dwarf varieties and increased fertilizer use. Semi-dwarfism is caused mutant wheat Reduced height-1 (Rht-1) rice semi-dwarf1 (sd1) alleles, respectively, which confer harvest index (grain to straw ratio) reduced yield loss from “lodging” (flattening crops wind or rain). However, despite their obvious global food security benefits, underlying mechanisms via GR dwarfing alleles actually work remained unknown. This began change with molecular discovery Rht1 (Peng et al., 1999Peng J. Richards D.E. Hartley N.M. Murphy G.P. Devos K.M. Flintham J.E. Beales Fish L.J. Worland A.J. Pelica F. al.“Green revolution” genes encode gibberellin response modulators.Nature. 1999; 400: 256-261Crossref PubMed Scopus (1396) Google Scholar). Previous studies Arabidopsis thaliana had discovered DELLA proteins (DELLAs), key components mechanism enabling phytohormone (GA) promote growth. DELLAs are nuclear-localized growth inhibitors, GA promotes plant overruling growth-inhibitory activity 1997Peng Carol P. King K.E. Cowling R.J. Harberd N.P. GAI gene defines a signaling pathway that negatively regulates responses.Genes Dev. 1997; 11: 3194-3205Crossref (828) overrules targeting them for destruction ubiquitin-proteasome system (Sasaki 2003Sasaki A. Itoh H. Gomi K. Ueguchi-Tanaka M. Ishiyama Kobayashi Jeong D.H. An G. Kitano Ashikari al.Accumulation phosphorylated repressor an F-box mutant.Science. 2003; 299: 1896-1898Crossref (481) Analysis properties gai (GA-insensitive) was important initial catalyst these advances. Compared wild-type (WT) GAI, allele encodes protein (Figure 1A) lacking 17 amino acid segment portion eponymous domain. resistant GA-promoted proteasome-dependent destruction, hence accumulates genetically dominant semi-dwarfism Rht-B1b Rht-D1b like gai, also GA-insensitive dwarfism. Rht-1 revealed Rht-D1b, again DELLA-encoding Scholar; see predicted encoded compared WT Rht-B1a Figure 1A). Later, SD1 shown biosynthetic GA20-oxidase, sd1 GA20-oxidase activity, bioactive levels, consequent accumulation SLR1 2002Sasaki Nishimura Swapan D. Saito T. Khush G.S. al.Green revolution: gibberellin-synthesis rice.Nature. 2002; 416: 701-702Crossref (794) Spielmeyer 2002Spielmeyer W. Ellis M.H. Chandle P.M. Semidwarf (sd-1), "green revolution" rice, contains defective 20-oxidase gene.Proc. Natl. Acad. Sci. U S 99: 9043-9048Crossref (573) Li 2018Li S. Tian Y. Wu Ye Yu Zhang Liu Q. Hu Tong al.Modulating growth-metabolism coordination sustainable agriculture.Nature. 2018; 560: 595-600Crossref (200) These advances begun solve mystery how work: through enhanced accumulation. Nevertheless, major puzzle remained. open reading frames both contain premature stop codons shortly following translation initiation AUG codon Scholar) At first sight mutations might be expected prevent into functional protein. considered gain-of-function repressors signaling. To explain this apparent discrepancy, Peng Scholar proposed translational reinitiation at alternative methionine start closely could generate N-terminally truncated Such would likely semi-dwarfism, other domain (e.g., gai; maize d8/mpl1; Although supported observation disrupting sequence encoding C-terminal region (named GRAS domain) suppresses dwarf phenotype (Mo 2018Mo Pearce Dubcovsky Phenotypic transcriptomic characterization tall carrying induced mutation PFYRE motif RHT-B1b.BMC Plant Biol. 18: 253Crossref (10) Scholar), hypothesis untested level many years. new report now provides test (Van De Velde 2021Van Thomas S.G. Heyse Kaspar R. Van Der Straeten Rohde N-terminal RHT-1 generated cause semi-dwarfing alleles.Mol. Plant. 2021; https://doi.org/10.1016/j.molp.2021.01.002Abstract Full Text PDF (8) First, expression constructs designed express tagged versions transgenic confers semi-dwarfism. Second, generates degradation, presumably observed phenotype. Further experiments hypothesis, phenotypes conferred putative short peptide initiated original terminating Transgenic immunologically detectable levels no effect on height, indicating unlikely correct. Thus, although relatively inefficient, responsible conferring phenotypes. study solves another puzzle. seed germination overcoming dormancy stimulating aleurone secretion α-amylase enzyme mobilizes endosperm starch reserves. In consequence, not only dwarfism, but blocks GA-induced (Fu 2001Fu X. Sudhakar J Christou Expression represses multiple responses.Plant Cell. 2001; 13: 1791-1802Crossref (85) Similarly, severely Rht-B1c allele, containing 30 insertion blocking DELLA, which, because its severity, has been used breeding, contrast, dwarfism without affecting either How discrepancies resolved? indicates they due differential regulation shoots aleurone. Translational shoots, thus while lack cells permits response. Conversely, acts independently shoot Semi-dwarf require high inorganic nitrogen (N) input achieve grain yield. Despite undeniable benefits GR, associated N inputs have extensive environmental damage. A post-GR agriculture must therefore build upon reducing use, maintaining increasing N-mediated responses N-use efficiency (NUE), impacts balancing multi-level interactions GRF4 NGR5 (Li 2020Wu Wang Song Chen al.Enhanced green revolution nitrogen-responsive chromatin modulation rice.Science. 2020; 367: eaaz2046Crossref knowledge active makes possible breeding strategies improved exhibiting NUE 1B), impact. For example, retain conserved LHR1 1A), supports interaction transcription factors including CRISPR-Cas9 mutagenesis affinity NGR5, improving and/or branching response, respectively. leave unaltered, Rht-B1b/RhtD1b expressed 1B). affect growth-regulatory factors, causing unwanted yield-beneficial strategy specifically mutate LHR1-interacting regions themselves, enhancing interaction. enhance (specifically NGR5), reduce Rht-B1b/Rht-D1b, unaltered enable precision having higher yields sustainability world agriculture.