LTR retrotransposon insertion inside CsERECTA for a LRR receptor-like Serine/threonine-protein kinase results in compact (cp) plant architecture in cucumber

Authors: CHEN, FEIFAN - University Of Wisconsin; YONG, JIANPENG - Northwest A&f University; ZHANG, GAOYUAN - Gansu Agricultural Uiversity; LIU, MENGYING - Northwest A&f University; WANG, QIQI - Northwest A&f University; ZHONG, HUILI - Northwest A&f University; PAN, YUPENG - University Of Wisconsin; CHEN, PENG - Northwest A&f University; Weng, Yiqun; LI, YUHONG - Northwest A&f University

Submitted to: Journal of Theoretical and Applied Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/26/2022
Publication Date: 3/9/2023
Citation: Chen, F., Yong, J., Zhang, G., Liu, M., Wang, Q., Zhong, H., Pan, Y., Chen, P., Weng, Y., Li, Y. 2023. LTR retrotransposon insertion inside CsERECTA for a LRR receptor-like Serine/threonine-protein kinase results in compact (cp) plant architecture in cucumber. Journal of Theoretical and Applied Genetics. Article number 31. https://doi.org/10.1007/s00122-023-04273-6.
DOI: https://doi.org/10.1007/s00122-023-04273-6

Interpretive Summary: Background: Plant height is an important architecture attribute affecting crop yield and quality. The cucumber compact (cp) mutation may have a potential to be used in cucumber breeding to develop cucumber ideotype. A previous study mapped the cp locus on cucumber chromosome 4, but the underlying gene is unknown. Major findings: We conducted map-based cloning and functional characterization of the cp gene. Fine genetic mapping in a very large population (nearly 10000 F2 plants) delimited the target gene into a very small region that contains only one gene named CsERECTA (CsER in short) that encodes a receptor-like kinase. The compact outlook is due to the insert of a large piece of DNA inside the CsER gene which disrupts its function. While there is no difference in its expression in the mutant and the regular wild type cucumber plants, when this normal cucumber gene was introduced into a mutant Arabidopsis plant in which the ER gene has been mutated, its expression can recover the dwarf plants caused by loss-of-function mutation in Arabidopsis ERECTA gene. The transcriptomes of the mutant and wild type cucumber plants were investigated with RNA-seq, which identified major phytohormone biosynthesis/signaling pathways regulated by the CsER gene in plant growth and development. Why it matters: Our work provides new insights into the molecular basis of compact plant formation in cucumber and other cucurbit crops. This work also facilitates marker-assisted selection for appropriate architecture in cucumber breeding.

Technical Abstract: Plant height is an important plant architecture trait. The compact (cp) mutant may have a potential to be used in cucumber breeding to manipulate cucumber ideotype. A previous study mapped the cp locus on cucumber chromosome 4. In this study, we reported map-based cloning and functional characterization of the cp gene. Fine genetic mapping with over 9500 F2 plants delimited the cp locus in an 8.8-kb region that contains only one candidate gene, CsERECTA (CsER) encoding an LRR receptor-like kinase. Sequence analysis revealed the insertion of a 5.5-kb long terminal repeat (LTR) retrotransposon in exon 22 resulting in loss of function of CsER in the mutant. CsER was highly expressed in the shoot apical meristem (SAM) and young organs, but there was no difference in its expression between the cucumber wild type and mutant. Ectopic expression of CsER driven by its own promoter indicated that CsER expressed in SAM, inflorescence, stem, leaf veins and stomata of transgenic Arabidopsis plants. The introduction of CsER could completely rescue the dwarf plant of Arabidopsis er105 mutant which is due to loss-of-function of AtERECTA whereas the compact inflorescence and small rosette leaves in this mutant could be partially recovered. Transcriptome profiling with RNA-seq in the cp mutant and the wild type plants revealed major phytohormone biosynthesis/signaling pathways regulated by CsER in plant growth and development. Findings from this study provide new insights into the molecular functions of the well-studied ERECRTA gene in plants. This work also helps efficient use of the cp mutant in cucumber breeding.