A single amino acid substitution in MdLAZY1A dominantly impairs shoot gravitropism in Malus

Authors: DOUGHTERY, LAURA - Cornell University; BOREJSZA-WYSOCKA, EWA - Cornell University; MIAULE, ALEXANDRE - Cornell University; WANG, PING - Cornell University; ZHENG, DESEN - Cornell University; JANSEN, MICHAEL - Cornell University; BROWN, SUSAN - Cornell University; Pineros, Miguel; DARDICK, CHRISTOPHER - Cornell University; XU, KENONG - Cornell University; MONAGHAN, JACQUELINE - Queen'S University - Canada; CHABOT, DENISE - Agriculture And Agri-Food Canada; SUBRAMANIAM, RAJAGOPAL - Agriculture And Agri-Food Canada; BLACKWELL, BARBARA - Agriculture And Agri-Food Canada; HARRIS, LINDA - Agriculture And Agri-Food Canada

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/4/2023
Publication Date: 7/3/2023
Citation: Doughtery, L., Borejsza-Wysocka, E., Miaule, A., Wang, P., Zheng, D., Jansen, M., Brown, S., Pineros, M., Dardick, C., Xu, K., Monaghan, J., Chabot, D., Subramaniam, R., Blackwell, B., Harris, L. 2023. A single amino acid substitution in MdLAZY1A dominantly impairs shoot gravitropism in Malus. Plant Physiology. https://doi.org/10.1093/plphys/kiad373.
DOI: https://doi.org/10.1093/plphys/kiad373

Interpretive Summary: This study highlights the importance of plant architecture in crop yield potential and productivity, specifically focusing on the role of downward branch bending in resource allocation. Downward bending is known to promote reproductive growth, favoring the formation of flowers and fruits over vegetative growth, such as branches and leaves. This study identified a mutation in a gene that leads to a drooping architecture of apple tree branches, which could affect the way the tree allocates resources. Redirection of resources toward reproductive structures has positive implications for improving orchard fruit productivity, quality, and orchard management.

Technical Abstract: Plant architecture is one of the most important factors that determine crop yield potential and productivity. In apple (Malus), genetic improvement of tree architecture has been challenging due to a long juvenile phase before flowering and their growth as complex trees comprising a distinct scion and a rootstock. In this study, the dominant weeping growth phenotype was investigated better to understand the genetic control of apple tree architecture. We report the identification of MdLAZY1A (MD13G1122400) as the genetic determinant underpinning the Weeping (W) locus that largely controls weeping growth in Malus. MdLAZY1A is one of the four paralogs in apple that are most closely related to AtLAZY1, involved in gravitropism in Arabidopsis. The weeping allele (MdLAZY1A-W) contains a single nucleotide mutation, c.584T>C, that results in a leucine to proline (L195P) residue substitution within a predicted transmembrane domain in Region III, one of the five conserved regions in LAZY1-like proteins. Subcellular localization revealed that MdLAZY1A is expressed at the plasma membrane and nucleus in plant cells. Over-expressing the weeping allele in cultivar Royal Gala (RG) with standard growth resulted in an impaired gravitropic response and altered the growth to weeping-like. Suppressing the standard allele (MdLAZY1A-S) by RNA interference (RNAi) in RG similarly changed the branch growth into a downward direction. Overall, the L195P mutation in MdLAZY1A is genetically causal for weeping growth, underscoring not only the crucial roles of residue L195 and Region III in MdLAZY1A-mediated gravitropic response, but also a potential DNA base editing target for tree architecture improvement in Malus.