# Editorial: Desiccation tolerance in land plants: from mechanisms to evolution

Xiaoshuang Li, Bei Gao, Andrew Wood, Julia Buitink, Daoyuan Zhang, Melvin Oliver

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## To cite this version:

Xiaoshuang Li, Bei Gao, Andrew Wood, Julia Buitink, Daoyuan Zhang, et al. Editorial: Desiccation tolerance in land plants: from mechanisms to evolution. Frontiers in Plant Science, 2023, 14, 10.3389/fpls.2023.1210946. [hal-04733540](https://hal.inrae.fr/hal-04733540v1)

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OPEN ACCESS

EDITED BY
Yongjiang Zhang,
University of Maine, United States

REVIEWED BY
Helen Holmlund,
Pepperdine University, United States
Chinese Academy of Sciences (CAS), China
Shi-jian Yang,
Yunnan University, China

*CORRESPONDENCE

Melvin J. Oliver

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olivermj@umsystem.edu

†These authors have contributed equally to this work

RECEIVED 23 April 2023

ACCEPTED 20 June 2023

PUBLISHED 27 June 2023

CITATION

Li X, Gao B, Wood AJ, Buitink J, Zhang D and Oliver MJ (2023) Editorial: Desiccation tolerance in land plants: from mechanisms to evolution.
*Front. Plant Sci.* 14:1210946.
doi: 10.3389/fpls.2023.1210946

COPYRIGHT

© 2023 Li, Gao, Wood, Buitink, Zhang and Oliver. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). 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: Desiccation tolerance in land plants: from mechanisms to evolution

Xiaoshuang Li¹†, Bei Gao¹,²†, Andrew J. Wood³†, Julia Buitink⁴†, Daoyuan Zhang¹† and Melvin J. Oliver⁵*

¹State Key Laboratory of Desert and Oasis Ecology, Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China, ²Xinjiang Key Laboratory of Conservation and Utilization of Plant Gene Resources, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China, ³Department of Plant Biology, Southern Illinois University-Carbondale, Carbondale, IL, United States, ⁴Université d'Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, France,

⁵Division of Plant Sciences and Technology, Interdisciplinary Plant Group, University of Missouri, Columbia, MO, United States

KEYWORDS

desiccation tolerance, editorial, special topic, resurrection plants, evolution

## Editorial on the Research Topic

### Desiccation tolerance in land plants: from mechanisms to evolution

Desiccation tolerance (DT) is the ability to survive and recover from the equilibration of the water potential of cellular contents to that of the surrounding air. Most plants resist water loss and have evolved strategies to maintain their cellular water potential above that of the surrounding air and are desiccation sensitive with cellular water potentials of -3 to -6 MPa generally lethal. Desiccation-tolerant plants allow the equilibration of the water potential of their cells to that of the air and can tolerate tissue water potentials of -100 MPa and lower (Alpert and Oliver, 2002). Most seeds, pollen and spores are also desiccation tolerant.

Vegetative desiccation tolerance (VDT) was present in early bryophytes (Oliver et al., 2005), suggesting acquisition of desiccation tolerance was critical for the colonization of the land by primitive plants (Mishler and Churchill, 1985). Phylogenetic evidence indicates that VDT was lost during the evolution of tracheophytes but has reappeared in the lycophyte, fern, and angiosperm lineages (Mishler and Churchill, 1985; Oliver et al., 2020). Desiccation tolerance in seeds (SDT) appeared subsequent to its loss during tracheophyte evolution. SDT differs from VDT in that it is part of a developmental program that directs loss of water during seed maturation. SDT, along with dormancy, enabled both gymnosperms and angiosperms to disperse and establish in almost every terrestrial ecosystem. VDT in angiosperms evolved in at least thirteen lineages spanning both dicots and monocots (Gaff and Oliver, 2013) and there is growing evidence that VDT in the angiosperms evolved from SDT by a 'rewiring' of the controlling genetic networks (Farrant and Moore, 2011; VanBuren, 2017).

SDT was critical for the rise of civilization and global human expansion *via* its role in plant domestication (Diamond, 2002; Purugganan, 2019; Schaal, 2019). The continued
importance of DT, both seed and vegetative, lies in understanding
the mechanisms that enable cells to withstand dehydration and
recover (Oliver et al., 2020). The hope is that within these processes
novel strategies for improving crop stress tolerance will emerge: a
vital need for a changing climate. The greatest promise comes from
investigations into the genomic aspects of desiccation tolerance and
recent whole genome sequencing of desiccation tolerant plants
(http://desiccation.egi.ac.cn/) offer new insights into both the
evolution of DT and the mechanisms and gene networks that
control it (González-Morales et al., 2016; VanBuren et al., 2018).

Although we have made significant progress in understanding
how plants tolerate desiccation (Oliver et al., 2020) there is still
much to learn and many questions to be answered. It was with this
in mind that we selected the topic of 'Desiccation tolerance in land
plants: from mechanisms to evolution' for this Research Topic.

In an enlightening review of the studies of the seeds of the
xerophytic plant *Caragana korshinski*, *Peng et al.* built a strong case
for the use of xerophytic seeds for uncovering the underlying
mechanisms of SDT. They also advocated for the positive aspects
of re-establishment of DT in germinating seeds as a means for
studying important regulatory aspects of DT. Staying with SDT,
*Sano et al.* investigated chromatin dynamics during the short post-
germination period in *Medicago trunculata* seeds when desiccation
tolerance can be re-induced by a PEG treatment before being
irretrievably lost as the seedling develops. They provided
convincing evidence that PEG stimulated a more open
configuration of the chromatin encompassing a number of
induced DT related genes. They also demonstrated that an
increase in H3K27me3 marking was associated with termination
of the developmental window within which DT could be
re-induced.

Barthlott et al. demonstrated biofilms of the desiccation-tolerant cyanobacterium *Hassallia byssoidea* are superhydrophobic (repels water), a property that enhances gas exchange and excludes competitors. Superhydrophobicity, restricted to biological surfaces, was suggested to be an evolutionary innovation during the colonization of the land. The presence of the superhydrophobic surface of a cyanobacterial biofilm suggested that this property may have an early prokaryotic Precambrian origin. They demonstrated the presence of superhydrophobic surfaces in all land plants and offered an argument for rethinking the role of superhydrobicity in plant evolution.

Three of the remaining articles focused on desiccation tolerance
in bryophytes. Yang et al. investigated a comprehensive time course
analysis of the dehydrating and rehydrating transcriptomes of
gametophytes of the DT biocrust moss *Syntrichia caninervis*.
Their analysis highlighted the accumulation of transcripts related
to cellular protection during desiccation, in particular transcripts of
oxidative metabolism, and the decline in transcripts associated with
photosynthesis. Rehydration reversed this trend. The analysis
highlighted the importance of several transcription factor families
in the desiccation rehydration response. Fang et al. investigated the
integrative response of the transcriptome and metabolome of the
Antarctic moss *Pohlia nutans* to a PEG imposed water deficit stress.

Almost half of the differentially changed metabolites were
flavonoids and lipids and those transcripts that integrated well
with the metabolite data were for flavonoid and long-chain fatty
acid biosynthesis genes. The third article focuses on evolution of the
abiotic stress responsive C2H2-type zinc finger proteins (C2H2-
ZFPs) along with a comparison of the expression characteristics of
these gene in *Physcomitrium patens* and Arabidopsis during
dehydration and rehydration. Li et al., in a comprehensive study,
demonstrated a general increase in C2H2-ZFP genes as plant
complexity increased, with *Physcomitrium* exhibiting a larger
number than expected likely related to the whole genome
duplication event that occurred in its evolutionary history.
Expression profiles for the C2H2-ZFPs of *Physcomitrium* and
Arabidopsis during dehydration and rehydration exhibited
different patterns of transcript accumulation reflecting both the
phylogenetic relationships and types of conserved promoter
domains; Z-type in non-seed plants and Q-type in seed plants.
These differences highlighted the desiccation tolerance and
sensitivity of these two plants.

Our remaining manuscript from Liu et al. explored the potential
of a dehydration responsive transcription factor, DREB A-5, from
the desiccation tolerant moss *Syntrichia caninervis* for crop
improvement. They demonstrated that ectopic expression of a
moss 35S-DREB A-5 construct improved germination rates and
seedling salt tolerance. Overexpression Arabidopsis lines had
enhanced levels of antioxidant enzymes and increased transcript
abundance of stress related genes, including the salt overly sensitive
(SOS) gene transcripts, SOS 1, 2 and 3. They provide convincing
evidence that the DREB 5-A improved salt tolerance in part by
stimulating jasmonic acid production.

Author contributions

All authors listed have made a substantial, direct, and
intellectual contribution to the work and approved it
for publication.

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.

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
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References

Alpert, P., and Oliver, M. J. (2002). "Drying without drying," in *Desiccation and plant survival*. Eds. M. Black and H. W. Pritchard (Wallingford, UK: Oxford University Press), pp3–p44.

Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. *Nature* 418, 700–707. doi: 10.1038/nature01019

Farrant, J. M., and Moore, J. P. (2011). Programming desiccation-tolerance: from plants to seeds to resurrection plants. *Cur. Opin. Plant Biol.* 14, 340–345. doi: 10.1016/j.pbi.2011.03.018

Gaff, D. F., and Oliver, M. J. (2013). The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. *Func. Plant Biol.* 40, 315–328. doi: 10.1071/FP12321

González-Morales, S. I., Chávez-Montes, R. A., Hayano-Kanashiro, C., Alejo-Jacuinde, G., Rico-Cambron, T. Y., de Folter, S., et al. (2016). Regulatory network analysis reveals novel regulators of seed desiccation tolerance in arabidopsis thaliana. *Proc. Nat. Acad. Sci. U. S. A.* 113, E5232–E5241. doi: 10.1073/pnas.161098511

Mishler, B. D., and Churchill, S. P. (1985). Transition to a land flora: phylogenetic relationships of the green algae and bryophytes. *Cladistics* 1, 305–328. doi: 10.1111/j.1096-0031.1985.tb00431.x

Oliver, M. J., Farrant, J. M., Hilhorst, H. W. M., Mundree, S., Williams, B., and Bewley, J. D. (2020). Desiccation tolerance: avoiding cellular damage during drying and rehydration. *Ann. Rev. Plant Biol.* 71, 435–460. doi: 10.1146/annurev-arplant-071219-105542

Oliver, M. J., Velten, J., and Mishler, B. D. (2005). Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? *Integ. Comp. Biol.* 45, 788–799. doi: 10.1093/icb/45.5.788

Purugganan, M. D. (2019). Evolutionary insights into the nature of plant domestication. *Cur. Biol.* 29, R705–R714. doi: 10.1016/j.cub.2019.05.053

Schaal, B. (2019). Plants and people: our shared history and future. *Plants People Planet.* 1, 14–19. doi: 10.1002/ppp3.12

VanBuren, R. (2017). Desiccation tolerance: seedy origins of resurrection. *Nat. Plants*. 3, 1–2. doi: 10.1038/nplants.2017.46

VanBuren, R., Man Wai, C., Pardo, J., Giarola, V., Ambrosini, S., Song, X., et al. (2018). Desiccation tolerance evolved through gene duplication and network rewiring in lindernia. *Plant Cell*. 30, 2943–2958. doi: 10.1105/tpc.18.00517