The maize heterotrimeric G protein β subunit controls shoot meristem development and immune responses
Monday, 2020/01/27 | 06:03:47
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Qingyu Wu, Fang Xu, Lei Liu, Si Nian Char, Yezhang Ding, Byoung Il Je, Eric Schmelz, Bing Yang, and David Jackson
PNAS January 21, 2020 117 (3) 1799-1805 SignificanceCereal crops, such as maize, provide our major sources of food and feed. Crop productivity has been significantly improved by the selection of favorable architecture and development alleles; however, crops are constantly under attack from pathogens, which severely limits yield due to a defense–growth trade-off. Therefore, identifying key signaling regulators that control both developmental and immune signaling is critical to provide basic knowledge to maximize productivity. This work shows that the maize G protein β subunit regulates both meristem development and immune signaling and suggests that manipulation of this gene has the potential to optimize the trade-off between yield and disease resistance to improve crop yields. AbstractHeterotrimeric G proteins are important transducers of receptor signaling, functioning in plants with CLAVATA receptors in controlling shoot meristem size and with pathogen-associated molecular pattern receptors in basal immunity. However, whether specific members of the heterotrimeric complex potentiate cross-talk between development and defense, and the extent to which these functions are conserved across species, have not yet been addressed. Here we used CRISPR/Cas9 to knock out the maize G protein β subunit gene (Gβ) and found that the mutants are lethal, differing from those in Arabidopsis, in which homologous mutants have normal growth and fertility. We show that lethality is caused not by a specific developmental arrest, but by autoimmunity. We used a genetic diversity screen to suppress the lethal Gβ phenotype and also identified a maize Gβ allele with weak autoimmune responses but strong development phenotypes. Using these tools, we show that Gβ controls meristem size in maize, acting epistatically with G protein α subunit gene (Gα), suggesting that Gβ and Gα function in a common signaling complex. Furthermore, we used an association study to show that natural variation in Gβ influences maize kernel row number, an important agronomic trait. Our results demonstrate the dual role of Gβ in immunity and development in a cereal crop and suggest that it functions in cross-talk between these competing signaling networks. Therefore, modification of Gβ has the potential to optimize the trade-off between growth and defense signaling to improve agronomic production.
See: https://www.pnas.org/content/117/3/1799
Figure 1: CRISPR/Cas9 knockouts of ZmGB1 led to autoimmune phenotypes. (A) CRISPR/Cas9 editing of ZmGB1 produced different frameshift alleles. White boxes indicate 5′ and 3′ UTRs, black boxes indicate exons, and black lines indicate introns. The positions of guide RNAs are indicated by red arrows. (B) Zmgb1CR mutants were lethal at the seedling stage. The pictures were taken at 5, 10, and 12 d after seeds were sown in soil. (Upper) WT. (Lower) Zmgb1CR mutants. (Scale bar: 1 cm.) (C and D) Trypan blue (C) and DAB (D) staining of WT and Zmgb1CR mutants showed increased staining in the mutants. (E) PR1 and PR5 expression were up-regulated in the Zmgb1CR mutants, and both 5-d-old and 10-d-old Zmgb1CR mutants accumulated significantly more salicylic acid (SA) (F). For E and F, P = 0.0001, Student’s t test; n = 3. (G) YFP-SBP-ZmGB1 localizes to membranes in shoot meristems. (Upper) Leaf cells expressing YFP-SBP-ZmGB1 (green), counterstained with FM4-64 (red), both visible as a thin line and overlapped (yellow) around the cell. (Middle) Following plasmolysis, YFP-SBP-ZmGB1 (arrows) remained colocalized with FM4-64. (Lower) YFP-SBP-ZmGB1 expression was found throughout SAM and tassel inflorescence primordia. (Scale bars: 50 μm.) |
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