Phylogenomic Evidence for the Monophyly of Bryophytes and the Reductive Evolution of Stomata

Harris, Brogan J.; Harrison, C. Jill; Hetherington, Alistair M.; Williams, Tom A.

doi:10.1016/j.cub.2020.03.048

Cited by 181 publications

(194 citation statements)

References 98 publications

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“…The evolution of stomata in land plants, given a monophyletic-bryophytes phylogeny, is not so clear, but they are not a shared-derived character (synapomorphy) uniting the hornworts, mosses, and tracheophytes (Mishler and Churchill, 1984;Ruszala et al, 2011). Only if it is assumed that the probability of loss of stomata was greater than the probability of gain (a not unreasonable assumption, see Harris et al, 2020) then the evolution of stomata would be a synapomorphy uniting all the land plants, with losses in the liverworts and several early-branching moss lineages. Else, if stomata are not homologous among land plants, then they would have been gained independently in the hornworts, mosses, and tracheophytes.…”

Section: The First Land Plantsmentioning

confidence: 99%

The Chloroplast Land Plant Phylogeny: Analyses Employing Better-Fitting Tree- and Site-Heterogeneous Composition Models

et al. 2020

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The colonization of land by descendants of charophyte green algae marked a turning point in Earth history that enabled the development of the diverse terrestrial ecosystems we see today. Early land plants diversified into three gametophyte-dominant lineages, namely the hornworts, liverworts, and mosses, collectively known as bryophytes, and a sporophytedominant lineage, the vascular plants, or tracheophytes. In recent decades, the prevailing view of evolutionary relationships among these four lineages has been that the tracheophytes were derived from a bryophyte ancestor. However, recent phylogenetic evidence has suggested that bryophytes are monophyletic, and thus that the first split among land plants gave rise to the lineages that today we recognize as the bryophytes and tracheophytes. We present a phylogenetic analysis of chloroplast protein-coding data that also supports the monophyly of bryophytes. This newly compiled data set consists of 83 chloroplast genes sampled across 30 taxa that include chlorophytes and charophytes, including four members of the Zygnematophyceae, and land plants, that were sampled following a balanced representation of the main bryophyte and tracheophyte lineages. Analyses of non-synonymous site nucleotide data and amino acid translation data result in congruent phylogenetic trees showing the monophyly of bryophytes, with the Zygnematophyceae as the charophyte group most closely related to land plants. Analyses showing that bryophytes and tracheophytes evolved separately from a common terrestrial ancestor have profound implications for the way we understand the evolution of plant life cycles on land and how we interpret the early land plant fossil record.

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Section: The First Land Plantsmentioning

confidence: 99%

The Chloroplast Land Plant Phylogeny: Analyses Employing Better-Fitting Tree- and Site-Heterogeneous Composition Models

et al. 2020

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“…However, the possibility of convergent evolution of stomata across plant groups has also been argued (Raven, 2002;Pressel et al, 2014). Recent molecular and physiological analyses suggest that the mechanisms of stomatal function and development are broadly conserved across land plants (Chater et al, 2011(Chater et al, , 2016Ruszala et al, 2011;Doi et al, 2015;Lind et al, 2015;Caine et al, 2016;Harris et al, 2020). However, in earlier diverging lineages including the bryophytes, the divergent physiology and functions of stomata continue to be debated (Duckett et al, 2009;Chater et al, 2011Chater et al, , 2013Chater et al, , 2016Pressel et al, 2014;Field et al, 2015;Chen et al, 2016;McAdam and Brodribb, 2016;Hõrak et al, 2017;Grantz et al, 2019).…”

Section: Building Increasingly Robust Stomatal Developmental Modulesmentioning

confidence: 99%

Stomata and Sporophytes of the Model Moss Physcomitrium patens

et al. 2020

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Mosses are an ancient land plant lineage and are therefore important in studying the evolution of plant developmental processes. Here, we describe stomatal development in the model moss species Physcomitrium patens (previously known as Physcomitrella patens) over the duration of sporophyte development. We dissect the molecular mechanisms guiding cell division and fate and highlight how stomatal function might vary under different environmental conditions. In contrast to the asymmetric entry divisions described in Arabidopsis thaliana, moss protodermal cells can enter the stomatal lineage directly by expanding into an oval shaped guard mother cell (GMC). We observed that when two early stage P. patens GMCs form adjacently, a spacing division can occur, leading to separation of the GMCs by an intervening epidermal spacer cell. We investigated whether orthologs of Arabidopsis stomatal development regulators are required for this spacing division. Our results indicated that bHLH transcription factors PpSMF1 and PpSCRM1 are required for GMC formation. Moreover, the ligand and receptor components PpEPF1 and PpTMM are also required for orientating cell divisions and preventing single or clustered early GMCs from developing adjacent to one another. The identification of GMC spacing divisions in P. patens raises the possibility that the ability to space stomatal lineage cells could have evolved before mosses diverged from the ancestral lineage. This would have enabled plants to integrate stomatal development with sporophyte growth and could underpin the adoption of multiple bHLH transcription factors and EPF ligands to more precisely control stomatal patterning in later diverging plant lineages. We also observed that when P. patens sporophyte capsules mature in wet conditions, stomata are typically plugged whereas under drier conditions this is not the case; instead, mucilage drying leads to hollow sub-stomatal cavities. This appears to aid capsule drying and provides further evidence for early land plant stomata contributing to capsule rupture and spore release.

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“…Many reviews regarding A. thaliana cell divisions as well as the molecular factors (transcriptional regulators, signaling and scaffolding molecules, and cell cycle regulators) exist and thus will not be covered extensively here. Many fate factors appear to be conserved across phyla (Harris et al, 2020). The divisions that create anisocytic stomata such as those in A. thaliana are illustrated in Figure 4A.…”

Section: How Do Subsidiary Cells Arise?mentioning

confidence: 99%

Flanking Support: How Subsidiary Cells Contribute to Stomatal Form and Function

2020

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Few evolutionary adaptations in plants were so critical as the stomatal complex. This structure allows transpiration and efficient gas exchange with the atmosphere. Plants have evolved numerous distinct stomatal architectures to facilitate gas exchange, while balancing water loss and protection from pathogens that can egress via the stomatal pore. Some plants have simple stomata composed of two kidney-shaped guard cells; however, the stomatal apparatus of many plants includes subsidiary cells. Guard cells and subsidiary cells may originate from a single cell lineage, or subsidiary cells may be recruited from cells adjacent to the guard mother cell. The number and morphology of subsidiary cells varies dramatically, and subsidiary cell function is also varied. Subsidiary cells may support guard cell function by offering a mechanical advantage that facilitates guard cell movements, and/or by acting as a reservoir for water and ions. In other cases, subsidiary cells introduce or enhance certain morphologies (such as sunken stomata) that affect gas exchange. Here we review the diversity of stomatal morphology with an emphasis on multi-cellular stomata that include subsidiary cells. We will discuss how subsidiary cells arise and the divisions that produce them; and provide examples of anatomical, mechanical and biochemical consequences of subsidiary cells on stomatal function.

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Phylogenomic Evidence for the Monophyly of Bryophytes and the Reductive Evolution of Stomata

Abstract: Highlights d Land plants comprise two sister lineages, bryophytes and tracheophytes d Their common ancestor possessed complex stomata d Stomata were lost or reduced during the evolution of bryophytes d Liverwort air pores evolved following stomatal loss in the liverwort ancestor

Cited by 181 publications

References 98 publications

The Chloroplast Land Plant Phylogeny: Analyses Employing Better-Fitting Tree- and Site-Heterogeneous Composition Models

The Chloroplast Land Plant Phylogeny: Analyses Employing Better-Fitting Tree- and Site-Heterogeneous Composition Models

Stomata and Sporophytes of the Model Moss Physcomitrium patens

Flanking Support: How Subsidiary Cells Contribute to Stomatal Form and Function

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