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      Evolution and function of red pigmentation in land plants

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          Abstract

          Background

          Land plants commonly produce red pigmentation as a response to environmental stressors, both abiotic and biotic. The type of pigment produced varies among different land plant lineages. In the majority of species they are flavonoids, a large branch of the phenylpropanoid pathway. Flavonoids that can confer red colours include 3-hydroxyanthocyanins, 3-deoxyanthocyanins, sphagnorubins and auronidins, which are the predominant red pigments in flowering plants, ferns, mosses and liverworts, respectively. However, some flowering plants have lost the capacity for anthocyanin biosynthesis and produce nitrogen-containing betalain pigments instead. Some terrestrial algal species also produce red pigmentation as an abiotic stress response, and these include both carotenoid and phenolic pigments.

          Scope

          In this review, we examine: which environmental triggers induce red pigmentation in non-reproductive tissues; theories on the functions of stress-induced pigmentation; the evolution of the biosynthetic pathways; and structure–function aspects of different pigment types. We also compare data on stress-induced pigmentation in land plants with those for terrestrial algae, and discuss possible explanations for the lack of red pigmentation in the hornwort lineage of land plants.

          Conclusions

          The evidence suggests that pigment biosynthetic pathways have evolved numerous times in land plants to provide compounds that have red colour to screen damaging photosynthetically active radiation but that also have secondary functions that provide specific benefits to the particular land plant lineage.

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          Most cited references216

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          Salinity tolerance in halophytes.

          Halophytes, plants that survive to reproduce in environments where the salt concentration is around 200 mm NaCl or more, constitute about 1% of the world's flora. Some halophytes show optimal growth in saline conditions; others grow optimally in the absence of salt. However, the tolerance of all halophytes to salinity relies on controlled uptake and compartmentalization of Na+, K+ and Cl- and the synthesis of organic 'compatible' solutes, even where salt glands are operative. Although there is evidence that different species may utilize different transporters in their accumulation of Na+, in general little is known of the proteins and regulatory networks involved. Consequently, it is not yet possible to assign molecular mechanisms to apparent differences in rates of Na+ and Cl- uptake, in root-to-shoot transport (xylem loading and retrieval), or in net selectivity for K+ over Na+. At the cellular level, H+-ATPases in the plasma membrane and tonoplast, as well as the tonoplast H+-PPiase, provide the trans-membrane proton motive force used by various secondary transporters. The widespread occurrence, taxonomically, of halophytes and the general paucity of information on the molecular regulation of tolerance mechanisms persuade us that research should be concentrated on a number of 'model' species that are representative of the various mechanisms that might be involved in tolerance.
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            Reactive oxygen species, abiotic stress and stress combination.

            Reactive oxygen species (ROS) play a key role in the acclimation process of plants to abiotic stress. They primarily function as signal transduction molecules that regulate different pathways during plant acclimation to stress, but are also toxic byproducts of stress metabolism. Because each subcellular compartment in plants contains its own set of ROS-producing and ROS-scavenging pathways, the steady-state level of ROS, as well as the redox state of each compartment, is different at any given time giving rise to a distinct signature of ROS levels at the different compartments of the cell. Here we review recent studies on the role of ROS in abiotic stress in plants, and propose that different abiotic stresses, such as drought, heat, salinity and high light, result in different ROS signatures that determine the specificity of the acclimation response and help tailor it to the exact stress the plant encounters. We further address the role of ROS in the acclimation of plants to stress combination as well as the role of ROS in mediating rapid systemic signaling during abiotic stress. We conclude that as long as cells maintain high enough energy reserves to detoxify ROS, ROS is beneficial to plants during abiotic stress enabling them to adjust their metabolism and mount a proper acclimation response.
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              Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

              The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PAPERCLIP.
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                Author and article information

                Contributors
                Journal
                Ann Bot
                Ann Bot
                annbot
                Annals of Botany
                Oxford University Press (US )
                0305-7364
                1095-8290
                01 November 2022
                07 September 2022
                07 September 2022
                : 130
                : 5
                : 613-636
                Affiliations
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                Department of Agriculture, Food and Environment, University of Pisa , Italy
                The New Zealand Institute for Plant and Food Research Limited, Department of Chemistry, Otago University , Dunedin, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 92169, Auckland Mail Centre, Auckland 1142, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                The New Zealand Institute for Plant and Food Research Limited , Private Bag 11600, Palmerston North 4442, New Zealand
                School of Biological Sciences, Monash University , Melbourne, VIC, Australia
                Author notes
                For correspondence. E-mail kevin.davies@ 123456plantandfood.co.nz
                Author information
                https://orcid.org/0000-0001-5652-5015
                https://orcid.org/0000-0002-8579-529X
                https://orcid.org/0000-0003-4018-0694
                https://orcid.org/0000-0002-4709-4281
                Article
                mcac109
                10.1093/aob/mcac109
                9670752
                36070407
                e645792b-5291-4d01-9012-eb53f1fb6cba
                © The Author(s) 2022. Published by Oxford University Press on behalf of the Annals of Botany Company.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 09 July 2022
                : 05 May 2022
                : 05 September 2022
                : 22 August 2022
                : 21 September 2022
                Page count
                Pages: 24
                Funding
                Funded by: Cargill, DOI 10.13039/100004387;
                Funded by: Centre for Australian National Biodiversity Research, DOI 10.13039/501100001175;
                Categories
                Invited Review
                AcademicSubjects/SCI01080
                AcademicSubjects/SCI01130
                AcademicSubjects/SCI01210

                Plant science & Botany
                anthocyanin,antioxidant,auronidin,betalain,biosynthesis,evolution,flavonoid,photoprotection,photomodulation,stress

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