Parental dominance of the cleopatra mandarin parent in the citrandarin allotetraploid hybrid shapes root-mediated salt tolerance

Abstract

Data Availability Statement: The original data supporting this study are included in the article and Supplementary Data. Further inquiries can be directed to the corresponding authors. Raw sequencing data have been deposited at NCBI under the BioProject accession PRJNA1156330. Parent PO reference genome (V1.3) and annotation (V1.3.1) were downloaded from Phytozome (Peng et al., 2020) (https://phytozome-next.jgi.doe.gov/info/Ptrifoliata_v1_3_1). The CL genome was assembled as part of the pre-HLB project and a primary version of its upcoming annotation was used. Information can be found in Droc et al. (2024).International audiencencreasing water limitation and soil salinisation resulting from climate change negatively impacts plant growth and productivity, posing a significant challenge to citrus production. This highlights the need to develop new citrus rootstocks that can tolerate both abiotic and biotic stress. Polyploidy is a major driver of plant evolution that often enhances resilience to abiotic stressors, including salinity. In this study, we evaluated for the first time the salt stress response of a citrandarin hybrid derived from a Cleopatra mandarin and a trifoliate orange at two ploidy levels: diploid (2x) and allotetraploid (4x). Plants exposed to salt stress were analysed at physiological, biochemical, ion, and transcriptomic levels in leaves and roots. Using multifactorial, multivariate, and network approaches, we deciphered the complexity of the multilevel response of both 2x and 4x hybrids. Regardless of stress, ploidy level accounted for differences in photosynthetic performance as well as in the transcriptional regulation of secondary metabolism and inorganic nutrients in roots. Under salt stress, both 2x and 4x displayed a robust salt-tolerant phenotype with no visible damage, while activating profound and coordinated physiological, biochemical, and transcriptional reprogramming. However, marked divergence in their adaptive strategies was identified when evaluating the ploidy × stress interaction. The 2x genotype relied mainly on enhanced leaf antioxidant metabolism, whereas the 4x exhibited stronger root-centred regulation involving ion partitioning, osmoprotection, aquaporin expression, and antioxidant pathways. Comparison between orthologues of each citrandarin parent further revealed a transcriptional bias towards Cleopatra mandarin, which was reinforced by tetraploidy under salt stress. Altogether, our results show that tetraploidy amplifies parental root regulatory programmes, providing mechanistic insights and candidate markers for the development of salt-tolerant citrus rootstocks