# Editorial: Building climate resilient deciduous tree crops by deciphering winter dormancy

Shu Yu, Bénédicte Wenden, Louise Ferguson, Li Tian

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Shu Yu, Bénédicte Wenden, Louise Ferguson, Li Tian. Editorial: Building climate resilient deciduous tree crops by deciphering winter dormancy. Frontiers in Plant Science, 2024, 15, 10.3389/fpls.2024.1463405. hal-04733056

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OPEN ACCESS

EDITED AND REVIEWED BY
Leo Marcelis,
Wageningen University and Research,
Netherlands

*CORRESPONDENCE

Li Tian

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ltian@ucdavis.edu

RECEIVED 11 July 2024

ACCEPTED 12 July 2024

PUBLISHED 26 July 2024

CITATION

Yu S, Wenden B, Ferguson L and Tian L (2024) Editorial: Building climate resilient deciduous tree crops by deciphering winter dormancy.

Front. Plant Sci. 15:1463405.

doi: 10.3389/fpls.2024.1463405

COPYRIGHT

© 2024 Yu, Wenden, Ferguson and Tian. This is an open-access article distributed under the terms of the [Creative Commons Attribution License (CC BY)](https://creativecommons.org/licenses/by/4.0/). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Editorial: Building climate resilient deciduous tree crops by deciphering winter dormancy

Shu Yu¹, Bénédicte Wenden², Louise Ferguson¹ and Li Tian¹*

¹Department of Plant Sciences, University of California, Davis, Davis, CA, United States, ²INRAE, Univ. Bordeaux, UMR Biologie du Fruit et Pathologie 1332, Villenave d'Ornon, France

KEYWORDS

winter dormancy, tree crops, bud break, heat accumulation, climate change

Editorial on the Research Topic

Building climate resilient deciduous tree crops by deciphering winter dormancy

Buds of deciduous tree crops enter winter dormancy in response to shorter photoperiods and lower temperatures in the fall. Winter dormancy comprises successive phases of endodormancy and ecodormancy. The transition from endodormancy to ecodormancy requires the exposure of dormant buds to a certain amount of chilling temperatures, whereas heat accumulation in ecodormant buds is essential for the successful shift from dormancy to active growth in tree crops (Lang et al., 1987). While bud dormancy allows plants to withstand harsh winters, timely bud break ensures their successful regrowth and production. As such, the initiation, progression, completion, and regulation of bud winter dormancy and break have been widely recognized for their importance in the survival and productivity of tree crops. However, climate change, often associated with warmer winters and temperature fluctuations (Inouye, 2022; Grossman, 2023), poses significant challenges to these processes, as alterations in temperature patterns can disrupt the delicate balance in temperature necessary for optimal bud dormancy and break.

This Research Topic centers on the biochemical, genetic, physiological, and environmental regulation of bud winter dormancy and its break in various woody perennials, with a focus on the impact of climate change. It also explores breeding strategies to adapt to climate change, particularly rising winter temperatures. The eight articles encompass studies conducted on three continents, covering a range of crops including nut, fruit, ornamental, and beverage crops. They are briefly highlighted below.

Gabay and Flaishman reviewed recent advancements in genetic and genomic resources as well as roles of genes, phytohormones, and metabolites related to dormancy regulation in pear (Pyrus spp.). They discussed the need for developing new pear cultivars with low chilling requirements and the challenges in pear breeding due to extended juvenility. They further emphasized the importance of understanding the genetic and physiological factors controlling bud dormancy in pear breeding. To this end, they pointed out the utility of quantitative trait loci (QTLs) in understanding dormancy regulation and developing genetic markers for marker-assisted selection in breeding. Lastly, the authors suggested Mediterranean climates could be used to simulate future temperate region climates for pear breeding.
Japanese plum (Prunus salicina Lindl.) trees require specific temperature conditions during bud dormancy for proper flowering in the spring. These requirements vary among cultivars due to genetic diversity (Guerra et al., 2009). Guerrero et al. analyzed the adaptation of 21 Japanese plum cultivars to future climate conditions using empirical data and climate projection models to predict chilling and heat accumulation (Delgado et al., 2021; Fadón et al., 2023). They found that the region of Badajoz in Spain may face challenges in meeting chilling requirements for dormant buds due to reduced winter chill, potentially limiting Japanese plum cultivation in these areas.

Scion/rootstock combinations are commonly used in pecan [Carya illinoensis (Wangenh.) K. Koch] production. Kaur et al. investigated the impact of low temperatures (-2, 0, 2, and 4°C) on bud break, leaf growth, and flower growth in different pecan scion/rootstock combinations. Their research showed that the low-temperature tolerance of these combinations correlated with their usage of bark soluble sugars and starches, as well as woody tissue soluble sugars. This insight is valuable for making informed decisions about scion/rootstock combinations in pecan orchards.

Leveraging integrated metabolite and transcriptional analysis, two studies explored biochemical and physiological mechanisms underlying bud dormancy release. Tang et al. dissected the regulatory network of bud sprouting in tea [Camellia sinesis (L.) O. Kuntze] by comparing metabolic and transcriptional profiles at different developmental stages. Their results highlighted the roles of plant hormones, glucose metabolism, and reactive oxygen species scavenging in the regulation of tea bud sprouting. In particular, soluble sugar reserves and oxidative stress before sprouting, and hormone regulation by zeatin during sprouting, led to bud dormancy release and active bud growth. Yu et al. used transcriptome analysis to examine gene expression profiles in pistachio (Pistacia vera L.) buds exposed to different winter chill accumulation at three orchard locations. Their study revealed increased expression of genes encoding enzymes breaking down callose and starch in endodormant buds, which facilitates endodormancy release and subsequent growth. Additionally, the decreased expression of genes involved in abscisic acid (ABA) biosynthesis suggested that lower ABA levels promote bud endodormancy release; this finding was supported by the observation of higher levels of carotenoid precursors and lower ABA content in buds undergoing endodormancy release.

To decipher the signaling mechanisms involved in bud dormancy establishment and release, Gai et al. applied a calcium (Ca²⁺) chelator and a Ca²⁺ channel blocker to dormant tree peony (Paeonia suffruticosa Andr.) buds, which resulted in delays in chilling- and gibberellic acid (GA)-induced endodormancy release. However, when Ca²⁺ was reapplied, the delay was alleviated, suggesting the involvement of Ca²⁺ in this process. Furthermore, the increased expression of several candidate calcium sensor genes following chilling and GA treatment suggests a potential role for calcium in bud endodormancy release, although further investigation is needed to determine if calcium functions as a signaling molecule or a nutrient in this process.

To identify genes participating in the bud break process, Mao et al. focused their study on PsATL33, a gene encoding a RING-H2

finger protein. They previously discovered that PsATL33 exhibited differential expression in chilling-treated tree peony buds (Yuan et al., 2024). In this study, overexpression of PsATL33 in petunia (Petunia hybrida 'Mitchell Diploid') accelerated seed germination, increased leaf size, and promoted axillary bud growth. Conversely, transiently silencing of PsATL33 in tree peony delayed bud break and growth, suggesting its role in releasing seeds and buds from dormancy. Additionally, this research revealed a connection between PsATL33 expression and the production of bioactive GA. The investigation by Watson et al. employed targeted capture sequencing on apple (Malus domestica Borkh.) to identify single nucleotide polymorphism (SNP) markers for dormancy- and flowering-related genes, as well as those in the interval of a previously identified QTL implicated in bud break. Through Genome-wide association studies (GWAS) analysis of 239 apple cultivars using these SNP markers, a SNP in MdPRX10, a candidate peroxidase gene, was associated with late bud break. The authors observed that the expression pattern of MdPRX10 was modulated by exposure to chilling temperatures. They proposed that MdPRX10 integrates temperature cues in dormancy pathways through redox-mediated signaling and regulation of C-repeat binding factor (CBF) genes associated with cold tolerance.

Collectively, these studies have enhanced our understanding of the genetic, physiological, and environmental factors that regulate bud winter dormancy and break in tree crops. They have also provided valuable insights for breeding programs, orchard management, and climate adaptation strategies. By comparing dormancy break mechanisms among different fruit and nut species, both conserved and species-specific genes and pathways could be identified. Additionally, future investigations could harness advanced breeding methods such as genomic selection to improve breeding efficiency by predicting and selecting desirable traits associated with bud winter dormancy and break.

## Author contributions

SY: Writing - review & editing. BW: Writing - review & editing. LF: Writing - review & editing. LT: Writing - review & editing, Writing - original draft.

## Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. SY, LF, and LT are grateful for the funding support provided by the California Pistachio Research Board.

## Acknowledgments

The Guest Editors would like to thank all the authors who contributed to this Research Topic, as well as the reviewers, editors, and the editorial office for their valuable support.
## Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The authors declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

## Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

## References

Delgado, A., Dapena, E., Fernandez, E., and Luedeling, E. (2021). Climatic requirements during dormancy in apple trees from northwestern Spain - Global warming may threaten the cultivation of high-chill cultivars. *Eur. J. Agron.* 130, 126374. doi: 10.1016/j.eja.2021.126374

Fadón, E., Fernandez, E., Luedeling, E., and Rodrigo, J. (2023). Agroclimatic requirements and adaptation potential to global warming of Spanish cultivars of sweet cherry (*Prunus avium* L.). *Eur. J. Agron.* 145, 126774. doi: 10.1016/j.eja.2023.126774

Grossman, J. J. (2023). Phenological physiology: seasonal patterns of plant stress tolerance in a changing climate. *New Phytol.* 237, 1508–1524. doi: 10.1111/nph.18617

Guerra, M. E., Rodrigo, J., López-Corrales, M., and Wünsch, A. (2009). *S-RNase* genotyping and incompatibility group assignment by PCR and pollination experiments in Japanese plum. *Plant Breed.* 128, 304–311. doi: 10.1111/j.1439-0523.2008.01552.x

Inouye, D. W. (2022). Climate change and phenology. *WIREs Climate Change*. 13, e764. doi: 10.1002/wcc.764

Lang, G., Early, J., Martin, G. C., and Darnell, R. M. (1987). Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. *Hortscience*. 22, 371–377. doi: 10.21273/HORTSCI.22.3.371

Yuan, Y., Zeng, L., Kong, D., Mao, Y., Xu, Y., Wang, M., et al. (2024). Abscisic acid-induced transcription factor PsMYB306 negatively regulates tree peony bud dormancy release. *Plant Physiol.* 194, 2449–2471. doi: 10.1093/plphys/kiae014