BPB1 regulates rice (Oryza sative L.) panicle length and panicle branch development by promoting lignin and inhibiting cellulose accumulation

Abstract

Panicle structure is one of the most important agronomic traits directly related to rice yield. This study identified a rice mutant basal primary branch 1 (bpb1), which exhibited a phenotype of reduced panicle length and arrested basal primary branch development. In addition, lignin content was found to be increased while cellulose content was decreased in bpb1 young panicles. Map-based cloning methods characterized the gene BPB1, which encodes a peptide transporter (PTR) family transporter. Phylogenetic tree analysis showed that the BPB1 family is highly conserved in plants, especially the PTR2 domain. It is worth noting that BPB1 is divided into two categories based on monocotyledonous and dicotyledonous plants. Transcriptome analysis showed that BPB1 mutation can promote lignin synthesis and inhibit cellulose synthesis, starch and sucrose metabolism, cell cycle, expression of various plant hormones, and some star genes, thereby inhibiting rice panicle length, resulting in basal primary branch development stagnant phenotypes. In this study, BPB1 provides new insights into the molecular mechanism of rice panicle structure regulation by BPB1 by regulating lignin and cellulose content and several transcriptional metabolic pathways.

Supplementary information: The online version contains supplementary material available at 10.1007/s11032-023-01389-x.

Keywords: Cellulose; Lignin; Primary branch development arrest; Short panicle.

Fig. 1

Comparative analysis of phenotypes of mutant bpb1 and wild-type NIP. a Comparison of phenotypes between mature mutant bpb1 and wild-type NIP. Bar = 15 cm. b Comparison of spike between mature mutant bpb1 and wild-type NIP. Bar = 5 cm; c, d 7-day and 12-day mutants bpb1 were compared with wild-type NIP seedlings. Bars = 2 cm; e–n Comparative analysis of plant height, panicle length, no. of primary branches, no. of secondary branches, no. of grains per panicle, no. of tillers, no. of roots, total length, root diameter, and root volume of mutant bpb1 and wild-type NIP. *P < 0.05, **P < 0.01

Fig. 2

Comparative analysis of grain size between mutant bpb1 and wild-type NIP. a, b Comparative analysis of grain size of mutant bpb1 and wild NIP grain and brown grain. Bars = 1 cm; c–f and g–j Comparative analysis of grain length, grain width, garin thickness, and 1000-grain weight of mutant bpb1 and wild NIP grain and brown grain. *P < 0.05, **P < 0.01

Fig. 3

Comparative analysis of young panicle elongation development of mutant bpb1 and wild-type NIP. a, b, e Phenotypic statistics of young panicle elongation development of wild-type NIP. Bars = 3 cm; c, d, f phenotypic statistics of young panicle elongation development of mutant bpb1. The white arrow represents the primary branch with stagnant development at the base of the bpb1 panicle. Bars = 3 cm; g statistical analysis of panicle length of mutant bpb1 and wild-type NIP. *P < 0.05, **P < 0.01; h–j Statistical analysis of the length of the first, second and third primary branches in the lower part of young panicle of mutant bpb1 and wild-type NIP. *P < 0.05, **P < 0.01

Fig. 4

Mapping cloning of target control gene BPB1 of mutant bpb1. a Fine mapping of mutant bpb1 target control gene. On the short vertical line is the molecular marker name, and below the short vertical line is the number of exchange plants; b, c sequence analysis of BPB1 mutation sites in mutants bpb1 and bpb2. The red box shows the mutation position and termination codon position; d analysis of the expression of BPB1 in mutants bpb1 and bpb2. *P < 0.05, **P < 0.01; e Comparative analysis of protein 3D structure of BPB1 and BPB2 after mutation

Fig. 5

Evolutionary tree analysis of BPB1. a Evolutionary tree analysis of BPB1 in plants. Blue represents dicotyledonous plants and green represents monocotyledonous plants. b Evolutionary tree analysis of BPB1 in dicotyledonous model plant Arabidopsis and monocotyledonous model plant rice. Blue represents Arabidopsis and orange represents rice

Fig. 6

Transcriptome analysis of young panicle of mutant bpb1 and wild-type NIP. a, b BPB1 mutation regulates the differential enrichment expression analysis of the phentlpropanoid biosynsis and starch and sucrose metabolism pathway in the mutant bpb1 and wild-type NIP. The red box represents the up-regulation of gene expression, and the green box represents the down-regulation of gene expression. The number in the box represents log₂ of the differential gene. c Validation analysis of partial differential genes in differential enrichment pathway by qRT-PCR

Fig. 7

Determination of lignin and cellulose content in young panicle of mutant bpb1 and wild-type NIP. a Analysis of lignin content in young panicle of mutant bpb1 and wild-type NIP. *P < 0.05, **P < 0.01. b Analysis of cellulose content in young panicle of mutant bpb1 and wild-type NIP. *P < 0.05, **P < 0.01. c Analysis of soluble sugar content in young panicle of mutant bpb1 and wild-type NIP. *P < 0.05, **P < 0.01