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Title: LITTLELEAF (LL) encodes a WD40 repeat domain-containing protein associated with organ size variation in cucumber

Author
item YANG, LUMING - University Of Wisconsin
item LIU, HANQUANG - University Of Wisconsin
item ZHAO, JIANYU - China Agricultural University
item PAN, YUPENG - University Of Wisconsin
item CHENG, SIYUAN - Henan Agricultural University
item LIETZOW, CALVIN - University Of Wisconsin
item WEN, CHANGLONG - University Of Wisconsin
item ZHANG, XIAOLAN - China Agricultural University
item Weng, Yiqun

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/6/2018
Publication Date: 6/14/2018
Citation: Yang, L., Liu, H., Zhao, J., Pan, Y., Cheng, S., Lietzow, C.D., Wen, C., Zhang, X., Weng, Y. 2018. LITTLELEAF (LL) encodes a WD40 repeat domain-containing protein associated with organ size variation in cucumber. Plant Journal. 95:834-847. https://doi.org/10.1111/tpj.13991.
DOI: https://doi.org/10.1111/tpj.13991

Interpretive Summary: Plants employ tight genetic control to integrate intrinsic growth signals and environmental cues to enable organ growth to a defined size. Many regulators for cell proliferation and/or cell expansion contributing to organ size control have been identified, but the information remains fragmentary. In this study, we characterized a cucumber littleleaf (ll) mutant H19 which exhibited smaller leaves, flowers, fruits and seeds, yet produced more lateral branches than standard-sized leaf cucumber lines. The small organ size in H19 was due mainly to reduced cell proliferation. QTL analysis revealed co-localization of major-effect QTL for fruit length and diameter, fruit and seed weight, as well as multiple lateral branches with the LL locus; indicating pleiotropic effects of the LL gene. We show that LL encoded a WD40 repeat domain-containing protein. The predicted LL protein of H19 differed from the wild type by a single amino acid substitution in the second WD40 repeat, which was predicted to be in a DNA binding region. This amino acid residue in normal leaf lines was completely conserved in 108 cucumber lines as well as 33 other vascular plant genomes examined. The LL gene was originated well before the emergence of flowering plants but it was lost in the grass genome lineage. Transcriptome profiling with bulked segregant RNA-Seq revealed a complex regulatory network for LL-mediated organ size control which included several known organ size regulators as well as multiple hormone signaling or ubiquitination pathways. Data presented herein supported LL as a novel master organ size regulator in cucumber.

Technical Abstract: Plant organ size is under strict genetic control. Many regulators for cell proliferation and/or cell expansion contributing to organ size control have been identified, but the information remains fragmentary. In this study, we characterized a cucumber littleleaf (ll) mutant H19 which exhibited smaller leaves, flowers, fruits and seeds, yet produced more lateral branches than standard-sized leaf cucumber lines. The small organ size in H19 was mainly due to reduced cell proliferation. QTL analysis revealed co-localization of major-effect QTL for fruit length and diameter, fruit and seed weight, as well as multiple lateral branches with the LL locus suggesting pleiotropic effects of the LL gene. Through map-based cloning, we show that LL encoded a WD40 repeat domain-containing protein. The predicted LL protein of H19 differed from the wild type by a single amino acid substitution in the second WD40 repeat, which was predicted to be in a DNA binding region. This amino acid residue in normal leaf lines was completely conserved in 108 cucumber lines as well as 33 other vascular plant genomes examined. The LL gene was originated well before the emergence of flowering plants but it was lost in the grass genome lineage. Transcriptome profiling with bulked segregant RNA-Seq revealed a complex regulatory network for LL-mediated organ size control which included several known organ size regulators as well as multiple hormone signaling or ubiquitination pathways. Data presented herein supported LL as a novel master organ size regulator in cucumber.