The current division of Orthotrichum (Bryophyta) species with immersed stomata

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目前对于埋没气孔的正毛藓（Bryophyta）物种的分类分割

A atual divisão das espécies de Orthotrichum (Bryophyta) com estômatos imersos

La división actual de las especies de Orthotrichum (Bryophyta) con estomas inmersos.

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Molecular data do not support the current division of Orthotrichum (Bryophyta) species with immersed stomata

Sawicki J., Plasek V., Szczecinska M. (2011)

Jakub SAWICKI, Vítězslav PLÁŠEK, Monika SZCZECIŃSKA,

(Department of Botany and Nature Protection, University of Warmia and Mazury in Olsztyn, 10-727 Olsztyn, Poland)

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Journal of Systematics and Evolution 50(1): 12-24 – https://doi.org/10.1111/j.1759-6831.2011.00168.x –

https://onlinelibrary.wiley.com/doi/10.1111/j.1759-6831.2011.00168.x

Abstract  

Genetic relationships between 27 Orthotrichum species of the subgenera Orthotrichum and Pulchella were reconstructed using the internal transcribed spacer regions 1 and 2, the chloroplast trnH-psbA region, and intron–exon splice junction (ISJ) and inter-simple sequence repeats (ISSR) markers. A phylogenetic analysis did not reflect the current division of the subgenus Pulchella into the sections Diaphana, Pulchella, and Rivularia. Species of the section Rivularia did not form a monophyletic group, and the only markers that indicated the distinctness of the section Pulchella were ISJ and ISSR. The most genetically diverse section was Diaphana, whose species were divided into several clades. The only proper phylogenetic unit was the subgenus Orthotrichum. The applied markers revealed the process of cryptic speciation in species of both subgenera.

The occurrence of immersed stomata is probably related to arid environments during the early Oligocene to late Miocene, whereas the appearance of semi-immersed stomata might be associated with the mesic–xeric or semiarid environments during the middle Miocene to Pliocene

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沉浸气孔的出现可能与早渐新世到晚中新世的干旱环境有关，而半沉浸气孔的出现可能与中中新世到上新世的湿润-干旱或半干旱环境有关。

A ocorrência de estômatos imersos provavelmente está relacionada a ambientes áridos durante o início do Oligoceno até o final do Mioceno, enquanto o surgimento de estômatos semi-imersos pode estar associado a ambientes meso-xéricos ou semiáridos durante o meio do Mioceno até o Plioceno.

La aparición de estomas sumergidos probablemente está relacionada con entornos áridos durante el Oligoceno temprano hasta el Mioceno tardío, mientras que la aparición de estomas semi-sumergidos podría estar asociada con entornos mésicos-xéricos o semiáridos durante el Mioceno medio hasta el Plioceno.

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Phylogeny of Orthotrichum s.l. and Ulota s.l. (Orthotrichaceae, Bryophyta): Insights into stomatal evolution

Wang Q.-H., Dong S.-S., Zhang J.-L., Liu Y., Jia Y. (2020)

Qing-Hua Wang, Shan-Shan Dong, Jin-Long Zhang, Yang Liu, Yu Jia,

Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen and Chinese Academy of Sciences, Shenzhen, 518004 China

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093 China

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Journal of Systematics and Evolution 60(4): 876-900 – https://doi.org/10.1111/jse.12713 –

https://onlinelibrary.wiley.com/doi/10.1111/jse.12713

Abstract

Orthotrichum Hedw. s.l. and Ulota Mohr s.l. are two of the most speciose genera of the xerophytic moss family Orthotrichaceae. We reconstructed the phylogeny of these two genera using three data matrices: (i) organellar genomes and 33 taxa; (ii) six loci from three genomes and 144 taxa; and (iii) two plastid loci and 163 taxa. The present phylogeny, based on the maximum sampling of genes or taxa to date, generally confirms the new classification of Orthotrichum and Ulota, and indicated that all Ulota species, except Ulota phyllantha Brid., form a clade and three lineages comprise the cryptoporous Orthotrichum clade. We provided new morphological characters that support the present division of the two genera. Ancestral state reconstruction of stoma indicates that superficial stomata in Orthotrichum represent a plesiomorphic character and semi-immersed stomata were derived from immersed stomata. The results also suggest that immersed stomata independently arose once in Orthotrichum, whereas semi-immersed stomata probably arose more than once. Molecular dating analysis reveals that the occurrence of immersed stomata is probably related to arid environments during the early Oligocene to late Miocene, whereas the appearance of semi-immersed stomata might be associated with the mesic–xeric or semiarid environments during the middle Miocene to Pliocene. Ancestral state reconstruction of habitat indicates that the saxicolous habitat is apomorphic and independently evolved multiple times in Orthotrichum and Ulota, which supports the former hypothesis. Considering morphological statistics, the development of the cryptopore in Orthotrichum could provide increased resilience to dry habitats, and might promote their habitat shift during evolution.

Intercellular spaces and sporophyte water relations in bryophytes-two ignored dimensions (evolution of the stomatal apparatus)

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细胞间空间与苔藓体水分关系——被忽视的两个维度（气孔器的演化）

Espaços intercelulares e relações hídricas do esporófito em briófitas – duas dimensões ignoradas (evolução do aparelho estomático).

Espacios intercelulares y relaciones hídricas del esporofito en briófitos: dos dimensiones ignoradas (evolución del aparato estomático).

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The evolution of the stomatal apparatus: intercellular spaces and sporophyte water relations in bryophytes-two ignored dimensions

Duckett J. G., Pressel S. (2018)

Jeffrey G Duckett , Silvia Pressel ,

• Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK

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Philos Trans R Soc Lond B Biol Sci. 373(1739): 20160498 – doi: 10.1098/rstb.2016.0498 – PMID: 29254963 – PMCID: PMC5745334 –

https://pubmed.ncbi.nlm.nih.gov/29254963/

Abstract

Cryo-scanning electron microscopy shows that nascent intercellular spaces (ICSs) in bryophytes are liquid-filled, whereas these are gas-filled from the outset in tracheophytes except in the gametophytes of Lycopodiales. ICSs are absent in moss gametophytes and remain liquid-filled in hornwort gametophytes and in both generations in liverworts. Liquid is replaced by gas following stomatal opening in hornworts and is ubiquitous in moss sporophytes even in astomate taxa. New data on moss water relations and sporophyte weights indicate that the latter are homiohydric while X-ray microanalysis reveals an absence of potassium pumps in the stomatal apparatus. The distribution of ICSs in bryophytes is strongly indicative of very ancient multiple origins. Inherent in this scenario is either the dual or triple evolution of stomata. The absence, in mosses, of any relationship between increases in sporophyte biomass and stomata numbers and absences, suggests that CO₂ entry through the stomata, possible only after fluid replacement by gas in the ICSs, makes but a minor contribution to sporophyte nutrition. Save for a single claim of active regulation of aperture dimensions in mosses, all other functional and structural data point to the sporophyte desiccation, leading to spore discharge, as the primeval role of the stomatal apparatus.This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.

Evidence not only for a common origin of all stomata in extant plants but also for relatively simple stomata in the ancestral plant

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不仅为现存植物中所有气孔的共同起源提供证据，而且为祖先植物中相对简单的气孔提供了证据。

Evidência não apenas para uma origem comum de todos os estômatos nas plantas existentes, mas também para estômatos relativamente simples na planta ancestral

Evidencia no solo de un origen común de todos los estomas en las plantas existentes, sino también de estomas relativamente simples en la planta ancestral

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Liverwort bHLH transcription factors and the origin of stomata in plants

Chang G., Ma J., Wang S., Tang M., Zhang B., Ma Y., Li L., Sun G., Dong S., Liu Y., Zhou Y., Hu X., Song C.-P., Huang J. (2023)

• Guanxiao Chang
• Jianchao Ma
• Shuanghua Wang
• Mengmeng Tang
• Bo Zhang
• Yadi Ma
• Lijuan Li
• Guiling Sun
• Shanshan Dong
• Yang Liu
• Yun Zhou
• Xiangyang Hu
• Chun-Peng Song
• Jinling Huang

Current Biology 33(13): 2806-2813

https://doi.org/10.1016/j.cub.2023.05.050

Highlights

• •No evidence exists for bHLH Ia gene duplication in the ancestral land plant
• •The bHLH Ia/IIIb regulatory module is highly conserved in land plants
• •MpSMF and MpSCRM1/2 affect the development of the epidermis and gametangiophores
• •MpSMF weakly complements the functions of AtMUTE and AtFAMA

Summary

Stomata are distributed in nearly all major groups of land plants, with the only exception being liverworts. Instead of having stomata on sporophytes, many complex thalloid liverworts possess air pores in their gametophytes. At present, whether stomata in land plants are derived from a common origin remains under debate. 

In Arabidopsis thaliana, a core regulatory module for stomatal development comprises members of the bHLH transcription factor (TF) family, including AtSPCH, AtMUTE, and AtFAMA of subfamily Ia and AtSCRM1/2 of subfamily IIIb. Specifically, AtSPCH, AtMUTE, and AtFAMA each successively form heterodimers with AtSCRM1/2, which in turn regulate the entry, division, and differentiation of stomatal lineages. 

In the moss Physcomitrium patens, two SMF (SPCH, MUTE and FAMA) orthologs have been characterized, one of which is functionally conserved in regulating stomatal development.

We here provide experimental evidence that orthologous bHLH TFs in the liverwort Marchantia polymorpha affect air pore spacing as well as the development of the epidermis and gametangiophores. We found that the bHLH Ia and IIIb heterodimeric module is highly conserved in plants. Genetic complementation experiments showed that liverwort SCRM and SMF genes weakly restored a stomata phenotype in atscrm1, atmute, and atfama mutant backgrounds in A. thaliana. In addition, homologs of stomatal development regulators FLP and MYB88 also exist in liverworts and weakly rescued the stomatal phenotype of atflp/myb88 double mutant. These results provide evidence not only for a common origin of all stomata in extant plants but also for relatively simple stomata in the ancestral plant.

Mat-forming mosses structure the composition of vascular plant communities

Balancing positive and negative plant interactions: how mosses structure vascular plant communities

Gornall J. L., Woodin S. J., Jónsdóttir I. S., van der Wal R.  (2011)

Jemma L. Gornall, Sarah J. Woodin, Ingibjorg S. Jónsdóttir & René van der Wal,

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Oecologia 166: 769–782 – https://doi.org/10.1007/s00442-011-1911-6 –

https://link.springer.com/article/10.1007/s00442-011-1911-6#citeas

Abstract

Our understanding of positive and negative plant interactions is primarily based on vascular plants, as is the prediction that facilitative effects dominate in harsh environments. It remains unclear whether this understanding is also applicable to moss–vascular plant interactions, which are likely to be influential in low-temperature environments with extensive moss ground cover such as boreal forest and arctic tundra. In a field experiment in high-arctic tundra, we investigated positive and negative impacts of the moss layer on vascular plants. Ramets of the shrub Salix polaris, herb Bistorta vivipara, grass Alopecurus borealis and rush Luzula confusa were transplanted into plots manipulated to contain bare soil, shallow moss (3 cm) and deep moss (6 cm) and harvested after three growing seasons. The moss layer had both positive and negative impacts upon vascular plant growth, the relative extent of which varied among vascular plant species. Deep moss cover reduced soil temperature and nitrogen availability, and this was reflected in reduced graminoid productivity. Shrub and herb biomass were greatest in shallow moss, where soil moisture also appeared to be highest. The relative importance of the mechanisms by which moss may influence vascular plants, through effects on soil temperature, moisture and nitrogen availability, was investigated in a phytotron growth experiment. Soil temperature, and not nutrient availability, determined Alopecurus growth, whereas Salix only responded to increased temperature if soil nitrogen was also increased. We propose a conceptual model showing the relative importance of positive and negative influences of the moss mat on vascular plants along a gradient of moss depth and illustrate species-specific outcomes. Our findings suggest that, through their strong influence on the soil environment, mat-forming mosses structure the composition of vascular plant communities. Thus, for plant interaction theory to be widely applicable to extreme environments such as the Arctic, growth forms other than vascular plants should be considered.

The mosses may control ecosystem function through rapid nutrient uptake and through their effects on both the thermal environment of the soil and associated development of permafrost

The Role of Bryophytes in Nutrient Cycling in the Taiga

Oechel W. C., Van Cleve K. (1986)

In: Forest Ecosystems in the Alaskan Taiga – © Springer-Verlag New York Inc. 1986 – https://link.springer.com/chapter/10.1007/978-1-4612-4902-3_9

The reason why bryophytes lie at the lower end of the leaf economics spectrum is their strong nonstomatal diffusion conductance limitation to photosynthesis, which is driven by their specific anatomical characteristics

Anatomical constraints to nonstomatal diffusion conductance and photosynthesis in lycophytes and bryophytes

Carriquí M., Roig-Oliver M., Brodribb T. J., Coopman R., Gill W., Mark K., Niinemets Ü., Perera-Castro A. V., Ribas-Carbó M., Sack L., Tosens T., Waite M., Flexas J. (2019)

Marc Carriquí ¹, Margalida Roig-Oliver ¹, Timothy J Brodribb ², Rafael Coopman ³, Warwick Gill ⁴, Kristiina Mark ⁵, Ülo Niinemets ^5 6, Alicia V Perera-Castro ¹, Miquel Ribas-Carbó ¹, Lawren Sack ⁷, Tiina Tosens ⁵, Mashuri Waite ⁸, Jaume Flexas ¹,

• ¹Research Group on Plant Biology under Mediterranean Conditions, Universitat de les Illes Balears (UIB) – Instituto de Investigaciones Agroambientales y de Economía del Agua (INAGEA), Carretera de Valldemossa Km 7.5, 07122, Palma, Illes Balears, Spain.
• ²School of Biological Sciences, University of Tasmania, Hobart, TAS, 7001, Australia.
• ³Ecophysiology Laboratory for Forest Conservation, Instituto de Conservación, Biodiversidad y Territorio, Facultad de Ciencias Forestales y Recursos Naturales, Universidad Austral de Chile, Campus Isla Teja, Casilla 567, Valdivia, Chile.
• ⁴Tasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, 7001, Australia.
• ⁵Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, Tartu, 51006, Estonia.
• ⁶Estonian Academy of Sciences, Kohte 6, 10130, Tallinn, Estonia.
• ⁷Department of Ecology and Evolutionary Biology, University of California Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA, 90095, USA.
• ⁸Center for Regional System Analysis, Planning, and Development, Bogor Agricultural University, Bogor, 16153, Indonesia.

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New Phytol. 222(3): 1256-1270 – doi: 10.1111/nph.15675 – Epub 2019 Feb 3 – PMID: 30623444 –

https://pubmed.ncbi.nlm.nih.gov/30623444/

Abstract

Photosynthesis in bryophytes and lycophytes has received less attention than terrestrial plant groups. In particular, few studies have addressed the nonstomatal diffusion conductance to CO₂ g_nsd of these plant groups. Their lower photosynthetic rate per leaf mass area at any given nitrogen concentration compared with vascular plants suggested a stronger limitation by CO₂ diffusion. We hypothesized that bryophyte and lycophyte photosynthesis is largely limited by low g_nsd . Here, we studied CO₂ diffusion inside the photosynthetic tissues and its relationships with photosynthesis and anatomical parameters in bryophyte and lycophyte species in Antarctica, Australia, Estonia, Hawaii and Spain. On average, lycophytes and, specially, bryophytes had the lowest photosynthetic rates and nonstomatal diffusion conductance reported for terrestrial plants. These low values are related to their very thick cell walls and their low exposure of chloroplasts to cell perimeter. We conclude that the reason why bryophytes lie at the lower end of the leaf economics spectrum is their strong nonstomatal diffusion conductance limitation to photosynthesis, which is driven by their specific anatomical characteristics.

Vascular conduits in Polytrichum that resist buckling while transporting water under tension, and leaves capable of regulating transpiration, permitting photosynthetic gas exchange without cavitation inside the vascular system

Advanced vascular function discovered in a widespread moss

Brodribb T. J., Carriquí M., Delzon S., McAdam S. A., Holbrook N. M. (2020)

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Nature Plants 6: 273-279 –

https://www.nature.com/articles/s41477-020-0602-x

Abstract

The evolution of terrestrial plants capable of growing upwards into the dry atmosphere profoundly transformed the Earth. A transition from small, ‘non-vascular’ bryophytes to arborescent vascular plants during the Devonian period is partially attributed to the evolutionary innovation of an internal vascular system capable of functioning under the substantial water tension associated with vascular water transport. Here, we show that vascular function in one of the most widespread living bryophytes (Polytrichum commune) exhibits strong functional parallels with the vascular systems of higher plants. These parallels include vascular conduits in Polytrichum that resist buckling while transporting water under tension, and leaves capable of regulating transpiration, permitting photosynthetic gas exchange without cavitation inside the vascular system. The advanced vascular function discovered in this tallest bryophyte family contrasts with the highly inefficient water use found in their leaves, emphasizing the importance of stomatal evolution enabling photosynthesis far above the soil surface.

A common regulatory mechanism underlies setal and stomatal formation

Stomatal regulators are co-opted for seta development in the astomatous liverwort Marchantia polymorpha

Moriya K. C., Shirakawa M., Loue-Manifel J., Matsuda Y., Lu Y.-T., Tamura K., Oka Y., Matsushita T., Hara-Nishimura I., Ingram G., Nishihama R., Goodrich J., Kohchi T.,  Shimada T. (2023)

Kenta C. Moriya, Makoto Shirakawa, Jeanne Loue-Manifel, Yoriko Matsuda, Yen-Ting Lu, Kentaro Tamura, Yoshito Oka, Tomonao Matsushita, Ikuko Hara-Nishimura, Gwyneth Ingram, Ryuichi Nishihama, Justin Goodrich, Takayuki Kohchi, Tomoo Shimada,

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Nature Plants – https://doi.org/10.1038/s41477-022-01325-5 –

https://www.nature.com/articles/s41477-022-01325-5#citeas

Abstract

The evolution of special types of cells requires the acquisition of new gene regulatory networks controlled by transcription factors (TFs). In stomatous plants, a TF module formed by subfamilies Ia and IIIb basic helix–loop–helix TFs (Ia-IIIb bHLH) regulates stomatal formation; however, how this module evolved during land plant diversification remains unclear. Here we show that, in the astomatous liverwort Marchantia polymorpha, a Ia-IIIb bHLH module regulates the development of a unique sporophyte tissue, the seta, which is found in mosses and liverworts. The sole Ia bHLH gene, MpSETA, and a IIIb bHLH gene, MpICE2, regulate the cell division and/or differentiation of seta lineage cells. MpSETA can partially replace the stomatal function of Ia bHLH TFs in Arabidopsis thaliana, suggesting that a common regulatory mechanism underlies setal and stomatal formation. Our findings reveal the co-option of a Ia-IIIb bHLH TF module for regulating cell fate determination and/or cell division of distinct types of cells during land plant evolution.

In bryophytes ABA has the same function as in higher plants, e. g. stomatal closure

Abscisic acid and desiccation tolerance in mosses

Bopp M., Werner O., (1993)

Botanica Acta 106: 103–106 – https://doi.org/10.1111/j.1438-8677.1993.tb00344.x –

https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1438-8677.1993.tb00344.x

Abstract

In higher plants the phytohormone ABA is involved in processes that are connected to water deficit, like stomatal closure or desiccation tolerance.

In bryophytes, also containing ABA in their tissues, physiological functions remained uncertain for a long time. Quite recently, several papers have shown different effects of exogenously applied ABA: stomatal closure in Anthoceros, drought hardening in Funaria and production of the landform in Riccia. In all these cases the relevant conditions (water deficit) enhance the endogenous ABA level significantly. For induced desiccation tolerance, ABA serves as a mediator to induce specific proteins (dehydrins) strongly connected with this tolerance.

Therefore, it can be concluded that in bryophytes ABA has the same function as in higher plants. It acts as a mediator in stress conditions.