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, 110 (51), 20431-6

NAL1 Allele From a Rice Landrace Greatly Increases Yield in Modern Indica Cultivars

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NAL1 Allele From a Rice Landrace Greatly Increases Yield in Modern Indica Cultivars

Daisuke Fujita et al. Proc Natl Acad Sci U S A.

Abstract

Increasing crop production is essential for securing the future food supply in developing countries in Asia and Africa as economies and populations grow. However, although the Green Revolution led to increased grain production in the 1960s, no major advances have been made in increasing yield potential in rice since then. In this study, we identified a gene, SPIKELET NUMBER (SPIKE), from a tropical japonica rice landrace that enhances the grain productivity of indica cultivars through pleiotropic effects on plant architecture. Map-based cloning revealed that SPIKE was identical to NARROW LEAF1 (NAL1), which has been reported to control vein pattern in leaf. Phenotypic analyses of a near-isogenic line of a popular indica cultivar, IR64, and overexpressor lines revealed increases in spikelet number, leaf size, root system, and the number of vascular bundles, indicating the enhancement of source size and translocation capacity as well as sink size. The near-isogenic line achieved 13-36% yield increase without any negative effect on grain appearance. Expression analysis revealed that the gene was expressed in all cell types: panicles, leaves, roots, and culms supporting the pleiotropic effects on plant architecture. Furthermore, SPIKE increased grain yield by 18% in the recently released indica cultivar IRRI146, and increased spikelet number in the genetic background of other popular indica cultivars. The use of SPIKE in rice breeding could contribute to food security in indica-growing regions such as South and Southeast Asia.

Keywords: gene validation; marker-assisted breeding; pleiotropy; qTSN4.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Characterization of yield-related traits of a NIL for SPIKE. (A) Plant morphologies. (B) Panicle structures. (C) Flag leaves. (D) Cross-sections of panicle neck. (Scale bars: A, 20 cm; B, 10 cm; C, 5 cm; D, 500 µm.) (E–J) Comparisons between IR64 and NIL-SPIKE of spikelet number per panicle (n = 8) (E), flag leaf width (n = 9) (F), root dry weight at maturity (n = 10) (G), rate of chalkiness in brown rice (H), number of vascular bundles in panicle neck (n = 20) (I), and grain weight per m2 among two dry (DS) and wet seasons (WS) (J). Percentages above bars in J are yield increases of the NIL relative to IR64. Values are means, with whiskers showing SD. (SEM in J). Significant at ***0.1%; **1%; *5%; n.s., not significant.
Fig. 2.
Fig. 2.
Map-based cloning and expression analysis of SPIKE. (A) A high-resolution map narrowed the SPIKE locus to an 18.0-kbp region between Ind4 and Ind12. The candidate gene is indicated in red. The squares indicate an artifact of gene model prediction. Numbers below the map show the number of recombinants. (B) Semiquantitative expression analysis of SPIKE in culm, leaf, leaf sheath, and root of IR64 and NIL-SPIKE (NIL). (C and D) Production of GUS driven by the NIL-SPIKE promoter in cross-sections of crown roots and lateral roots (C) and young panicles (D). (Scale bars: C, 50 µm; D, 2 mm.) (E) Quantitative expression analysis of SPIKE in 3- to 5-, 6- to 10-, 11- to 20-, and 21- to 50-mm stages of young panicle of IR64 and NIL-SPIKE. Expression is calibrated to the 3- to 5-mm panicle stage of IR64. Values are means of three replications, with whiskers showing SEM. Significant at *5%; n.s., not significant.
Fig. 3.
Fig. 3.
Transgenic analysis for SPIKE through overexpression and gene silencing. (A) Morphologies of IR64 plant and Ubi:SPIKE plant in which SPIKE is overexpressed by the ubiquitin promoter. (B) Panicle structures of IR64 and Ubi:SPIKE. Spikelet number per panicle (C) and flag leaf width (D) of IR64 (n = 17) and Ubi:SPIKE plants carrying a single copy (n = 20) and five copies (n = 13). (E) Morphologies of NIL-SPIKE plant and transgenic plant in which SPIKE is silenced by amiRNA. (F) Panicle structures of NIL-SPIKE and transgenic plants. Spikelet number per panicle (G) and flag leaf width (H) of NIL-SPIKE (n = 5) and of amiRNA1 (n = 4) and amiRNA4 transgenic plants (n = 3). Values are means, with whiskers showing SD. Results of Tukey–Kramer test for multiple comparisons at the 5% level are shown in C, D, G, and H. (Scale bars: A and E, 20 cm; B and F, 5 cm.) Means labeled with different letters (a, b, c) differ significantly.
Fig. 4.
Fig. 4.
SPIKE increases grain yield in indica genetic background. (A and B) Gene location (blue ellipses) and plant morphology of New Plant Type cultivar YP4 (A) and IRRI146 and IRRI146-SPIKE (B). (Scale bars: 20 cm.) (C–E) Comparison between IRRI146 and IRRI146-SPIKE of grain weight per m2 (C), spikelet number per panicle (D), and flag leaf width (E) (n = 10). (F) Comparison of spikelet number per panicle between indica cultivars with and without SPIKE—PSBRc18 (from Philippines, n = 10), TDK1 (from Laos, n = 10), Ciherang (from Indonesia, n = 13), Swarna (from India, n = 17), and BR11 (from Bangladesh, n = 27)—characterized in the field at IRRI, Philippines. Values are means, with whiskers showing SE. Significant at ***0.1%; **1%; *5%.

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