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, 112 (1), 76-81

Rare Allele of a Previously Unidentified Histone H4 Acetyltransferase Enhances Grain Weight, Yield, and Plant Biomass in Rice

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Rare Allele of a Previously Unidentified Histone H4 Acetyltransferase Enhances Grain Weight, Yield, and Plant Biomass in Rice

Xian Jun Song et al. Proc Natl Acad Sci U S A.

Abstract

Grain weight is an important crop yield component; however, its underlying regulatory mechanisms are largely unknown. Here, we identify a grain-weight quantitative trait locus (QTL) encoding a new-type GNAT-like protein that harbors intrinsic histone acetyltransferase activity (OsglHAT1). Our genetic and molecular evidences pinpointed the QTL-OsglHAT1's allelic variations to a 1.2-kb region upstream of the gene body, which is consistent with its function as a positive regulator of the traits. Elevated OsglHAT1 expression enhances grain weight and yield by enlarging spikelet hulls via increasing cell number and accelerating grain filling, and increases global acetylation levels of histone H4. OsglHAT1 localizes to the nucleus, where it likely functions through the regulation of transcription. Despite its positive agronomical effects on grain weight, yield, and plant biomass, the rare allele elevating OsglHAT1 expression has so far escaped human selection. Our findings reveal the first example, to our knowledge, of a QTL for a yield component trait being due to a chromatin modifier that has the potential to improve crop high-yield breeding.

Keywords: grain size; plant biomass; rice; weight; yield.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
QTL cloning at GW6a. (AD) Grain and brown grain phenotypes. (E) QTL GW6 detection. A threshold of 2.0 as LOD (log likelihood) was used to declare the presence of significant QTL in a genomic region. (F) Graphical genotypes. (G) The candidate region of GW6 defined by markers xj112 and xj113. (H) GW6 consisted of two loci: GW6a, mapped between markers xj-6 and xj-11, and GW6b. (I) Fine-mapping of GW6a to a portion of Nipp PAC clone AP005453, where four recombinants were identified by using 3,012 plants. (J) Five annotated genes exist within the mapped region of ∼40 kb, and the Kasa genomic BAC clone K0242A07 and four sub-BACs for the transgenic assays are shown. (K) Progeny testing shows that the QTL GW6a effect is placed within a 4-kb interval. (L) Grain and brown grain phenotypes of indicated plants. (M) Comparisons of grain weight between plants shown in L. ***P < 0.001; Student’s t test was used to generate the P values in C, D, and M and a pairwise test was used to determine significance in K. (Scale bars: 3 mm.)
Fig. 2.
Fig. 2.
GW6a encodes a functional GNAT-like protein: OsglHAT1. (A) OsglHAT1 structure and mutation sites, including SNPs (blue) and changed amino acid residues (red). (B) Grain phenotypes of plants overexpressing the OsglHAT1 Nipp allele (OsglHAT1N-OE) and the Kasa allele (OsglHAT1K-OE), and OsglHAT1 antisense transgene (OsglHAT1-AS). (C) Comparison of grain weight. (D) Seed phenotypes of Arabidopsis plants overexpressing the OsglHAT1N-OE and OsglHAT1K-OE. (E) Comparison of seed weight of Arabidopsis transgenes. ***P < 0.001. Student’s t test was used to generate the P values in C and E.
Fig. 3.
Fig. 3.
Altered OsglHAT1 promoter activity underlies the QTL effect on grain weight regulation. (A) qPCR analysis of OsglHAT1 expression pattern. RNA was isolated and quantitated by qPCR, normalized to ubiquitin. CS, culm tissue containing shoot apical meristem; LB, leaf blade; LS, leaf sheath; PA, young panicle; RO, root. (B) Transient assay using maize leaf protoplasts to test OsglHAT1 promoter activity. GUS staining of transgenic samples containing pOsglHAT1N::GUS (C and E) and pOsglHAT1K::GUS construct (D and F). r, root hair. (G) Quantification of the GUS signal that harbors the construct as indicated. In situ RNA hybridization of OsglHAT1 shows expression in the vegetative stage (H and L) and during the reproductive stage (I, J, M, and N); (K and O) Negative controls of OsglHAT1 in situ RNA hybridization that uses a sense probe. (Scale bars: 100 μm.) The length of the promoters pOsglHAT1N and pOsglHAT1K used in BG was 1,681 and 1,652 bp, respectively, upstream of the ORF of OsglHAT1 alleles. Sample sections in HK are Nipp genotypes, and in LO are Kasa genotypes. *P < 0.1; **P < 0.05; ***P < 0.001. Student’s t test was used to generate the P values.
Fig. 4.
Fig. 4.
OsglHAT1 affects the number of cells in spikelet hulls and modulates grain yield and plant biomass. (A) Spikelet hull phenotypes used for SEM inspection. (B) Comparison of spikelet hull length between Nipp and NIL(OsglHAT1) at the same stage as A. (C) Histological examination in the central portion of inner epidermal cells of lemma by SEM. (Scale bars: 100 μm.) Double-headed arrows indicate cell lengths. (D) Comparison of inner epidermal cell length of Nipp (counted cells, n = 499) and NIL(OsglHAT1) (n = 496) lemmas. (E) Grain phenotypes. (F) Brown grain phenotypes. (G) Quantification and comparison of grain yield per plant. (H) Plant phenotypes of indicated plants at harvest. (I) Quantification and comparison of plant biomass per plant. ***P < 0.001; N.S., not significant. Data are given as the means ± SD, n > 20 plants in B, G, and I. Student’s t test was used to generate the P values.

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