Morpho-Physiological and Genomic Evaluation of Juglans Species Reveals Regional Maladaptation to Cold Stress

Abstract

Climate change may have unpredictable effects on the cold hardiness of woody species planted outside of their range of origin. Extreme undulations in temperatures may exacerbate susceptibility to cold stress, thereby interfering with productivity and ecosystem functioning. Juglans L. and their naturally occurring interspecific F1 hybrids, are distributed natively across many temperate regions, and J. regia has been extensively introduced. Cold hardiness, an environmental and genetic factor yet to be evaluated in many native and introduced Juglans species, may be a limiting factor under future climate change and following species introductions. We evaluated cold hardiness of native North American and Eastern Asian Juglans along with J. regia genotypes using field data from the Midwestern United States (Indiana), controlled freezing tests, and genome sequencing with close assessment of Juglans cold hardy genes. Many Juglans species previously screened for cold-hardiness were genotypes derived from the Midwest, California, and Europe. In 2014, despite general climate adaptation, Midwestern winter temperatures of −30 • C killed J. regia originating from California; however, naturalized Midwestern J. regia survived and displayed low damage. Hybridization of J. regia with black walnut (J. nigra) and butternut (J. cinerea) produced F1s displaying greater cold tolerance than pure J. regia. Cold hardiness and growth are variable in Midwestern J. regia compared to native Juglans, East Asian Juglans, and F1 hybrids. Phylogeny analyses revealed that J. cinerea sorted with East Asian species using the nuclear genome but with North American species using the organellar genome. Investigation of selected cold hardy genes revealed that J. regia was distinct from other species and exhibited less genetic diversity than native Juglans species Average whole genome heterozygosity and Tajima's D for cold hardy genes was low within J. regia samples and significantly higher for hybrid as well as J. nigra. We confirmed that molecular and morpho-physiological data were highly correlated and thus can be used effectively to characterize cold hardiness in Juglans species. We conclude that the genetic diversity within local J. regia populations is low and additional germplasm is needed for development of more regionally adapted J. regia varieties.

Cold and heat tolerances of hybrids for restoration of the endangered Juglans cinerea L

“…Consistent with other studies, this suggests that cold tolerance might be a heritable and possibly dominant trait, because the response of both hybrid types was closer to that of the most cold-tolerant parent, J. cinerea. These results align especially closely with those reported by Ebrahimi et al (2020) in a cold hardiness evaluation of seven Juglans species and their hybrids, including J. cinerea crossed with J. ailantifolia and J. regia. When less cold-tolerant species were crossed with more cold-tolerant species,…”

“…Thus, while J. cinerea and J. ailantifolia both experience average high summer temperatures of around 30 °C in the hottest parts of their distributions, J. ailantifolia lives in an overall warmer ecosystem than J. cinerea. Recently, Ebrahimi et al (2020) described higher cold tolerance of J. cinerea relative to J. ailantifolia. However, we are aware of no study that has compared their heat tolerances.…”

Unraveling genetic variation among white spruce families generated through different breeding strategies: Heritability, growth, physiology, hormones and gene expression

“…Future research should evaluate the response of trees, produced from different breeding strategies, to stressful conditions. It is also very likely that studies in biotechnology, phenomics, genomics, genome-wide associations and epigenetics will become essential methods in tree improvement programs, forest management and conservation practices since they allow for the identification of causal variants underlying phenotypes of interest, the evolutionary trajectory of populations to be studied, and help us understand the phenotypic plasticity and adaptive capacity of trees ( Faino and Thomma, 2014 ; Plomion et al., 2016 ; Lind et al., 2018 ; Sow et al., 2018 ; Ebrahimi et al., 2020 ; Mahony et al., 2020 ; Rellstab, 2021 ; Singh et al., 2021 ). Compared with agricultural crops, timely domestication of trees is almost unachievable through traditional genetic improvement methods alone, due to the long breeding cycles and rotation times ( Pearsall, 2008 ; Harfouche et al., 2012 ).…”

Genome-Wide Identification of the CBF Gene Family and ICE Transcription Factors in Walnuts and Expression Profiles under Cold Conditions

“…However, there is a limitation for pollinating quality and walnut yield in temperate regions where temperatures can plunge rapidly in the period of late spring frost (cold shock), especially in northern areas [ 28 , 29 , 30 ]. This extremely serious climate change can cause damage to the flower buds and even entire plants [ 31 , 32 , 33 ]. Climate change may affect the growth of woody tree species in their distribution region, as low temperatures affect plant development and growth in wild walnuts [ 23 , 30 ].…”

“…Climate change may affect the growth of woody tree species in their distribution region, as low temperatures affect plant development and growth in wild walnuts [ 23 , 30 ]. The developments in whole genome sequencing in walnut and woody species have revealed evidence of cold and chilling stress [ 28 , 31 , 32 , 33 , 34 ] and the genome-wide identification of gene families related to stress studies in Juglans species [ 35 , 36 , 37 , 38 ]. CBF and ICE1, as important transcription factors in response to cold stress, may enhance the cold resistance of plants under low-temperature conditions by regulating the essential functional genes [ 39 , 40 , 41 ].…”