Molecular basis of a shattering resistance boosting global dissemination of soybean

Hideyuki Funatsuki; Masaya Suzuki; Aya Hirose; Hiroki Inaba; Tetsuya Yamada; Makita Hajika; Kunihiko Komatsu; Takeshi Katayama; Takashi Sayama; Masao Ishimoto; Kaien Fujino

doi:10.1073/pnas.1417282111

Edited by Maarten J. Chrispeels, University of California, San Diego, La Jolla, CA, and approved October 30, 2014 (received for review September 12, 2014)

Significance

Pod dehiscence is a critical step in the seed dispersal (shattering) of legume and crucifer crops and can cause significant yield losses. Upon drying, pod walls are dehisced by two factors: the reduction of pod-wall binding strength and the generation of dehiscing forces. Although the previously reported shattering-resistant mutants maintained binding strength, here, we show a gene regulating the dehiscing force. The gene, Pdh1, encodes a dirigent family protein, known to be involved in lignification, which increases dehiscing forces by promoting torsion of dried pod walls. The loss-of-function pdh1 gene has been widely used as a shattering-resistance gene in soybean breeding. This knowledge could be useful in improving other legume and crucifer crops, as well as soybean breeding.

Abstract

Pod dehiscence (shattering) is essential for the propagation of wild plant species bearing seeds in pods but is a major cause of yield loss in legume and crucifer crops. Although natural genetic variation in pod dehiscence has been, and will be, useful for plant breeding, little is known about the molecular genetic basis of shattering resistance in crops. Therefore, we performed map-based cloning to unveil a major quantitative trait locus (QTL) controlling pod dehiscence in soybean. Fine mapping and complementation testing revealed that the QTL encodes a dirigent-like protein, designated as Pdh1. The gene for the shattering-resistant genotype, pdh1, was defective, having a premature stop codon. The functional gene, Pdh1, was highly expressed in the lignin-rich inner sclerenchyma of pod walls, especially at the stage of initiation in lignin deposition. Comparisons of near-isogenic lines indicated that Pdh1 promotes pod dehiscence by increasing the torsion of dried pod walls, which serves as a driving force for pod dehiscence under low humidity. A survey of soybean germplasm revealed that pdh1 was frequently detected in landraces from semiarid regions and has been extensively used for breeding in North America, the world’s leading soybean producer. These findings point to a new mechanism for pod dehiscence involving the dirigent protein family and suggest that pdh1 has played a crucial role in the global expansion of soybean cultivation. Furthermore, the orthologs of pdh1, or genes with the same role, will possibly be useful for crop improvement.

Footnotes

↵¹To whom correspondence may be addressed. Email: funazki{at}affrc.go.jp or kaien{at}res.agr.hokudai.ac.jp.

Author contributions: H.F. and K.F. designed research; H.F., M.S., A.H., H.I., T.Y., M.H., K.K., T.K., T.S., and K.F. performed research; H.F., T.K., M.I., and K.F. analyzed data; and H.F., T.K., M.I., and K.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database {DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank accession nos. AB823548 (Pdh1 full-length cDNA, cv. Toyomusume); AB826447 (3.4-kb Pdh1 genomic sequence of cv. Toyomusume transferred to cv. Jack); AB823549 (pdh1 sequence corresponding to coding sequence, cv. Hayahikari); AB823550 (Pdh1 coding sequence, cv. Misuzudaizu); AB823551 [ORF1 (Glyma16g25570.1), coding sequence, cv. Toyomusume]; AB823552 (ORF1 [Glyma16g25570.1], coding sequence, cv. Hayahikari); and AB823553 (partial sequence of BAC clone H88I22, cv. Misuzudaizu)}.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1417282111/-/DCSupplemental.