Suppressing a phosphohydrolase of cytokinin nucleotide enhances grain yield in rice

Jun 01, 2023

Nature Genetics (2023)Cite this article

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One-step and two-step pathways are proposed to synthesize cytokinin in plants. The one-step pathway is mediated by LONELY GUY (LOG) proteins. However, the enzyme for the two-step pathway remains to be identified. Here, we show that quantitative trait locus GY3 may boost grain yield by more than 20% through manipulating a two-step pathway. Locus GY3 encodes a LOG protein that acts as a 5′-ribonucleotide phosphohydrolase by excessively consuming the cytokinin precursors, which contrasts with the activity of canonical LOG members as phosphoribohydrolases in a one-step pathway. The residue S41 of GY3 is crucial for the dephosphorylation of iPRMP to produce iPR. A solo-LTR insertion within the promoter of GY3 suppressed its expression and resulted in a higher content of active cytokinins in young panicles. Introgression of GY302428 increased grain yield per plot by 7.4% to 16.3% in all investigated indica backgrounds, which demonstrates the great value of GY302428 in indica rice production.

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Sequence data from this study can be found in GenBank under accession number PRJEB6180, SRX502298–SRX502317 and SRX502162–SRX502255 for 3,010 diverse accessions, 20 African cultivated rice accessions and 94 accessions of O. barthii, respectively. The eChlp–seq sequence data and BED files were deposited in the NCBI Gene Expression Omnibus with accession number GSE231360. The reference genome of MH63RS2 and Nipponbare can be found in Rice Information GateWay (http://rice.hzau.edu.cn/rice_rs2/) and The Rice Annotation Project (https://rapdb.dna.affrc.go.jp/). All data are available in the main text or the Supplementary Information and Supplementary Data. Source data are provided with this paper.

All software used in the study are publicly available as described in Methods and Reporting Summary.

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We thank B. Han for sharing the clone An-2, M. J. Han for assistance in analyzing the retrotransposon structure and J. B. Wang for his excellent fieldwork. The computations in this paper were performed on the bioinformatics computing platform of the National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University. This work was partially supported by funds from the National Natural Science Foundation of China (31821005 to Q.Z., U20A2031 to Y.X., 32061143042 to Y.X. and 31901519 to X.Z.), the Earmarked Fund for China Agriculture Research System (CARS-01 to Q.Z.) and the National Key Laboratory of Crop Genetic Improvement Self-research Program (ZW22B0204 to Y.X.).

National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

Bi Wu, Jianghu Meng, Hongbo Liu, Donghai Mao, Huanran Yin, Zhanyi Zhang, Xiangchun Zhou, Bo Zhang, Ahmed Sherif, Xianghua Li, Jinghua Xiao, Wenhao Yan, Lei Wang, Xingwang Li, Wei Chen, Weibo Xie, Ping Yin, Qifa Zhang & Yongzhong Xing

Hubei Hongshan Laboratory, Wuhan, China

Bi Wu, Wenhao Yan, Lei Wang, Xingwang Li, Wei Chen, Weibo Xie, Ping Yin, Qifa Zhang & Yongzhong Xing

Hubei collaborative Innovation Center for Grain Industry, Yangtze University, Jingzhou, China

Haiyang Liu

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Y.X. conceived and supervised this study and reviewed and modified the manuscript. B.W. designed and performed the experiments, collected and analyzed the data and wrote the manuscript. J.M. collected young panicle samples. Hongbo Liu, H.Y. and W.C. measured the cytokinin contents. D.M. and A.S. developed the materials. Z.Z. conducted the eChlp–seq. X.Z. collected the indica backbone parents. B.Z. collected the phenotypic data of 533 accessions. Xianghua Li and J.X. organized the laboratory operations. Haiyang Liu, Xingwang Li, W.Y., W.X., P.Y., L.W. and Q.Z. contributed valuable suggestions for the manuscript. All the authors read and approved the manuscript.

Correspondence to Yongzhong Xing.

The authors declare no competing interests.

Nature Genetics thanks Hitoshi Sakakibara, Xiangdong Fu and Yuling Jiao for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

a–d, Comparison of whole plant (a), panicle (b), primary branch (c) and panicle architecture (d) between 02428 and 02428-GY3TQ at maturation stage. Bars, 5 cm. e–q, Performance of grain yield per plant (e), secondary branches per panicle (f), spikelets per panicle (g), grains per panicle (h), plant height (i), tillers per plant (j), heading date (k), primary branches per panicle (l), panicle length (m), 1000-grains weight (n), seed setting rate (o), biomass weight per plant (p) and harvest index (q) between 02428 and 02428-GY3TQ. r, Relative expression level of GY3 in leaves at seedling stage. Data are means ± SE (n = 30 for e–q, n = 3 for r). P values were calculated by two-sided paired Student’s t-test.

Source data

a–d, Performances of whole plant (a), panicle (b), branch (c) and panicle architecture (d) of TQ, TQ-GY302428 and their hybrids with G46B at maturation stage, Bars, 5 cm. e, Genetic constitution of TQ-GY302428 identified by 6 K SNP array. f, Relative expression level of GY3 in TQ, TQ-GY302428 and their hybrids with G46B in leaves at seedling stage. g, Grain yield per plot of TQ and TQ-GY302428. Data are mean ± SE (n = 3 for f, n = 6 for g); P values were calculated by two-sided paired Student’s t-test.

Source data

a, Gene structure and sequence variations between 02428 and TQ alleles. b, Schematic representation of the complementing (CP) and over-expressing (OE) constructs of GY3. c–n, Comparisons of yield-related traits including grain yield per plant (c), secondary branches per panicle (d), spikelets per panicle (e), grains per panicle (f), tillers per plant (g), primary branches per panicle (h),1000-grains weight (i), panicle length (j), seed setting rate (k), biomass per plant (l), harvest index (m) and plant height (n) between 02428 and 02428-CP lines. For box plots in c–n, the box limits indicate the 25th and 75th percentiles, whiskers further extend by ±1.5 times the interquartile range from the limits of each box, and the center line indicates the median, individual data points are plotted (n = 29, 29, 23 and 21 for 02428, 02428-CP_1, 02428-CP_2 and 02428-CP_3, respectively). P values were calculated by two-sided paired Student’s t-test.

Source data

a–d, Comparisons of whole plant (a), panicle (b), primary branch (c) and panicle architecture (d) between 02428 and 02428-OE plant. Bars, 5 cm. (e) Expression level of GY3 in the leaves of 02428 and 02428-OE plants at seedling stage. Data are means ± SE (n = 4). f–q, Performances of tillers per plant (f), primary branches per panicle (g), secondary branches per panicle (h), panicle length (i), spikelets per panicle (j), grains per panicle (k) 1000-grains per plant (l), seed setting rate (m), grain yield per plant (n), biomass per plant (o), harvest index (p) and plant height (q) of 02428 and 02428-OE plants. For box plots in f–q, the box limits indicate the 25th and 75th percentiles, whiskers further extend by ±1.5 times the interquartile range from the limits of each box, and the center line indicates the median, individual data points are plotted (n = 29, 30, 32 and 29 for 02428, 02428-OE_1, 02428-OE_2 and 02428-OE_3, respectively). P values were calculated by two-sided paired Student’s t-test.

Source data

a–d, Comparisons of whole plant (a), panicle (b), and panicle architecture (c) between ZH11 and ZH11GY3-KO plant. Bars, 5 cm. d–h, Performance of spikelets per panicle (d), primary branches per panicle (e), secondary branches per panicle (f), tillers per plant (g), panicle length (h) between ZH11 (n = 12) and ZH11GY3-KO (n = 13) T0 plants with varied insertions or deletions resulted GY3 loss-of-function. Data are means ± SE. (i), The cytokinin contents in young leaves of ZH11 and ZH11GY3-KO plants. Data are means ± SE (n = 3). P values were calculated by two-sided paired Student’s t-test. n.d. represents not detected.

Source data

a, b, Comparisons of cytokinin contents including DHZ (a) and DHZR (b) in young panicles of 02428, 02428-GY3TQ, 02428-CP, 02428-OE, and 02428LTR-KO. Data are means ± SE (three biological and three technical replicates). Different letters upon the bars indicated significant difference at P < 0.01 via Duncan test (a and b). c, Detection of the enzyme-catalysed reaction products of GY3 (red) and An-2 (blue) to iP and iPR, respectively. Std, standards of iPRMP, iP and iPR. d, Enzymatic product molar mass ratio of iP to iPR in An-2 (I), GY3 (IX) and mixtures with a molar mass ratio of An-2 to GY3 from 27:1 to 1:27 in 3-fold increments (from II to VIII with 27:1, 9:1, 3:1, 1:1, 1:3, 1:9, 1:27, respectively). e, Detection the enzyme-catalysed reaction products of newly recombinant enzymes (A-B-III, A-II-C, I-II-C, I-B-C, I-B-III). Std, standards of iPRMP, iP and iPR.

Source data

a, The expression patterns of GY3 in 02428 and 02428-GY3TQ plants. Data are means ± SE (n = 3). P values were calculated by two-sided paired Student’s t-test. b–g, RNA in situ hybridization of GY3 by anti-sense probes in inflorescence meristems at primary branch initiating stage (b and e), secondary branching formation stage (c and f) and floral meristem developing stage (d and g) between 02428 (b, c and d) and 02428-GY3TQ (e, f and g). (h), the signals of sense probe of GY3 in 02428 were used as the negative control. Bars, 20 μm.

Source data

a–d, Performances of whole plant (a), panicle (b), branch (c) and panicle architecture (d) of MH63, MH63-GY302428 and their hybrids crossed with G46B at maturation stage. Bars, 5 cm. e, Genetic components of MH63-GY302428 identified by the 6 K SNP array. f, Relative expression level of GY3 in leaves at seedling stage. g, Comparison of grain yield per plot (each plot contained 40 plants) of MH63, MH63-GY302428 and their hybrids crossed with G46B. Data are mean ± SE (n = 3). P values were calculated by two-sided paired Student’s t-test.

Source data

a–d, Performances of whole plant (a), panicle (b), branch (c) and panicle architecture (d) of SH527, SH527-GY302428 and their hybrids crossed with G46B at maturation stage. Bars, 5 cm. e, Genetic components of SH527-GY302428 identified by the 6 K SNP array. f, Relative expression level of GY3 in leaves at seedling stage. g, Comparisons of grain yield per plot (each plot contained 40 plants) of SH527, SH527-GY302428 and their hybrids crossed with G46B. Data are mean ± SE (n = 3); P values were calculated by two-sided paired Student’s t-test.

Source data

Illustration of the substrate-binding cavities of An-2 (a) and GY3 (d) with docking its substrate iPRMP, the structure of An-2 and GY3 are predicted by AlphaFold. (b and e) show the hydrogen bond and its lengths between riboside of iPRMP and its interaction amino acid residues in An-2 (b) and GY3 (e). (c and f) show the hydrogen bond and its lengths between the phosphate of iPRMP and its interaction amino acid residues in An-2 (c) and GY3 (f). Residues involved in enzyme catalysis, AMP-binding residues show as red and green sticks, respectively. The yellow dash lines represent the hydrogen bond and the number adjacent to each bond represent hydrogen bond lengths. The red dash lines (e and f) represent lengths between atoms in GY3 catalysis residue for the corresponding hydrogen bond formation in An-2.

Supplementary Figs. 1–7 and Tables 1–7.

Source data for Supplementary Figs. 1, 4 and 5.

Supplementary Data 2: Solo-LTR genotype list of 533 Oryza sativa accessions based PCR products. 3: Solo-LTR genotype list of AA genome Oryza species based on WGS. 4: Solo-LTR genotype list of African cultivated rice based on WGS. 5: Solo-LTR genotype list of 3,010 rice population based on WGS. 6: Solo-LTR genotype list of backbone lines for hybrids in China based on PCR products. 7: Primer used in this study.

Statistical source data.

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Wu, B., Meng, J., Liu, H. et al. Suppressing a phosphohydrolase of cytokinin nucleotide enhances grain yield in rice. Nat Genet (2023). https://doi.org/10.1038/s41588-023-01454-3

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Received: 11 August 2022

Accepted: 21 June 2023

Published: 27 July 2023

DOI: https://doi.org/10.1038/s41588-023-01454-3

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