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A frameshift mutation in JAZ10 resolves the growth versus defense dilemma in rice
Saturday, 2025/01/04 | 06:52:52

Lei-Lei LiYujie XiaoBaohui WangYunqi ZhuangYumeng ChenJing LuYonggen Lou, and Ran Li

PNAS; December 18 2024; 121 (52) e2413564121; https://doi.org/10.1073/pnas.2413564121

Significance

The insertion-deletions (INDELs) of unpredictable length at the target site introduced by CRISPR-Cas9-based genome editing potentially alter the gene’s coding frame and result in novel proteins. To date, few studies have focused on the characterization of these proteins. The phytohormone jasmonate (JA) plays a central role in plant resistance to herbivores. Here, we found that mutations in a rice JA suppressor gene OsJAZ10 by CRISPR-Cas9-based genome editing did not affect canonical JA signaling. However, a frameshift protein generated by a type of OsJAZ10 mutant confers plant resistance to herbivores without yield penalty in the laboratory and field, representing an alternative solution to uncouple rice growth–defense trade-offs. INDEL-based mutagenesis can be used to discover proteins with applications in plant breeding.

Abstract

CRISPR-Cas9 genome editing systems have revolutionized plant gene functional studies by enabling the targeted introduction of insertion-deletions (INDELs) via the nonhomologous end-joining (NHEJ) pathway. Frameshift-inducing INDELs can introduce a premature termination codon and, in other instances, can lead to the appearance of new proteins. Here, we found that mutations in the rice jasmonate (JA) signaling gene OsJAZ10 by CRISPR-Cas9-based genome editing did not affect canonical JA signaling. However, a type of mutant with an INDEL that yielded a novel frameshift protein named FJ10 (Frameshift mutation of JAZ10), exhibited enhanced rice growth and increased resistance to brown planthopper attacks. Overexpression of FJ10 in wild-type plants phenocopies OsJAZ10 frameshift mutants. Further characterization revealed that FJ10 interacts with Slender Rice 1 (OsSLR1) and F-box/Kelch 16 (OsFBK16). These interactions disrupt the function of OsSLR1 in suppressing gibberellin-mediated growth and the function of OsFBK16 in repressing lignin-mediated defense responses, respectively. Field experiments with FJ10-expressing plants demonstrate that this protein uncouples the growth–defense tradeoff, opening broad avenues to obtain cultivars with enhanced yield without compromised defenses.

 

See https://www.pnas.org/doi/10.1073/pnas.2413564121

 

Figure 1: Frameshift mutation of OsJAZ10 affects rice growth and BPH resistance (A) Mean transcript levels (±SE, n = 3 to 5) of OsJAZ10 in BPH-treated and control wild-type (WT) plants. Asterisks indicate significant differences between control and treatment (**P < 0.01; ***P < 0.001; Student’s t test). (B) Mutation of OsJAZ10 by CRISPR-Cas9-based genome editing. Two target sites were used, and the mutations in those sites were listed. (C) Amino acid alignment of wild-type OsJAZ10 and OsJAZ10 mutants created by genome editing. Highly conserved sequences of the domain and motif were marked. The predicted cryptic MYC-interacting domain (CMID) is highlighted in green, the TIFY motif in blue, and the Jas domain in yellow. The initial frameshift site is in red font. (D) Mean hatching rate (±SE, n = 12) of BPH eggs on jaz10 mutants and WT plants. The leaf sheath experimental setup used in BPH bioassays was shown in the Left panel. (E) Growth phenotype of jaz10 mutants and WT plants at the seedling stage. Photographs were taken ten days after germination. (Scale bar, 5 cm.) Mean plant height and leaf sheath length (± SE, n = 10) were shown. (F and G) Growth phenotype and yield of jaz10 mutants and WT plants in the field under control conditions. Photographs were taken 110 d after planting. (Scale bar, 20 cm.) Mean plant height, leaf sheath length (±SE, n = 7 to 10), and yield per plant (± SE, n = 18 to 21) are shown. Letters indicate significant differences among mutants and WT plants (P < 0.05, one-way ANOVA, followed by Tukey’s post hoc tests).

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