Gudrun Kadereit

Phylogeny of Amaranthaceae and Chenopodiaceae and the Evolution of C4 Photosynthesis

A phylogenetic analysis of Chenopodiaceae and Amaranthaceae was carried out using sequence variation of the chloroplast gene rbcL. Our sampling included 108 species of these two families along with 29 species of Caryophyllales serving as outgroups. Phylogeny inferences with maximum parsimony and maximum likelihood indicate that the two families form a well‐supported monophyletic clade that is sister to Achatocarpaceae. Despite extensive sampling, we found that the relationship between Chenopodiaceae and Amaranthaceae remains unclear as a result of short and weakly supported basal branches. The clearly monophyletic Polycnemoideae (traditionally considered a subfamily of Chenopodiaceae) appear as sister to Amaranthaceae sensu stricto. Within Amaranthaceae, most major lineages inferred except Gomphrenoideae and Celosieae do not correspond to recognized subfamilies and tribes. Bosea and Charpentiera branch first in the Amaranthaceae. Within Chenopodiaceae, the genera of Betoideae occur in basal and largely unresolved positions. The remaining Chenopodiaceae are divided into three major clades of unclear relationship: Chenopodioideae (Atripliceae s.str., Chenopodieae I‐III); Corispermoideae (Corispermeae); and Salicornioideae (Haplopeplideae, Salicornieae), Suaedoideae (Suaedeae, Bienertieae), and Salsoloideae (Camphorosmeae, Sclerolaeneae, Salsoleae I‐II). The rbcL tree is discussed also with regard to historical classifications and morphological support for the major clades. The molecular results are used to elucidate the evolution of C4 photosynthesis in the two families. C4 photosynthesis has evolved independently at least three times in Amaranthaceae and at least 10 times in Chenopodiaceae. A survey of C4 leaf anatomy revealed 17 different leaf types that in most cases mark an independent origin of C4 photosynthesis. The application of a molecular clock indicates an age of C4 photosynthesis of 11.5–7.9 Ma in Atriplex (Chenopodioideae) and 21.6–14.5 Ma in subfamily Salsoloideae.

Molecular phylogeny of Atripliceae (Chenopodioideae, Chenopodiaceae): Implications for systematics, biogeography, flower and fruit evolution, and the origin of C4 photosynthesis.

UNLABELLED PREMISE OF THE STUDY Atripliceae (Chenopodiaceae), including Atriplex (300 spp.) as the largest genus of the family, are an ecologically important group of steppes and semideserts worldwide. Relationships in Atripliceae are poorly understood due to obscure and potentially convergent morphological characters. • METHODS Using sequence variation of two chloroplast markers (rbcL gene, atpB-rbcL spacer) and one nrDNA marker (ITS) analyzed with BEAST, we investigated the systematics and biogeography of Atripliceae. We surveyed flower morphology and fruit anatomy to study the evolution of flowers and fruits in the tribe. • KEY RESULTS Female flowers with persistent foliar cover (the diagnostic character of traditional Atripliceae) evolved three times in Chenopodioideae, in Atripliceae s.s., Axyrideae, and Spinacia. Atripliceae s.s. started to diversify during the Early Miocene in Eurasia, separating into the Archiatriplex and the Atriplex clades. The former consists of eight species-poor, disjunct, and morphologically heterogeneous genera and is likely a relictual lineage. The Atriplex clade comprises the majority of species and evolved one C(4) lineage 14.1-10.5 Ma, which diversified rapidly worldwide. The C(4) Atriplex entered North America during the Middle/Late Miocene and spread to South America subsequently. Australia was colonized by two C(4) lineages both arriving during the Late Miocene. One of them diversified rapidly, giving rise to most Australian Atriplex species. • CONCLUSIONS Atripliceae s.s. comprise Archiatriplex, Atriplex, Exomis, Extriplex, Grayia, Halimione, Holmbergia, Manochlamys, Proatriplex, and Stutzia. Microgynoecium is included based on morphology but only weak molecular support. Axyris, Krascheninnikovia, and Ceratocarpus (here described as Axyrideae) and Spinacia are excluded from Atripliceae.

A taxonomic nightmare comes true: phylogeny and biogeography of glassworts (Salicornia L., Chenopodiaceae)

In this study we analysed ETS sequence data of 164 accessions belonging to 31 taxa of Salicornia, a widespread, hygrohalophytic genus of succulent, annual herbs of Chenopodiaceae subfam. Salicornioideae, to investigate phylogenetic and biogeographical patterns and hypothesise about the processes that shaped them. Furthermore, our aim was to understand the reasons for the notorious taxonomic difficulties in Salicornia. Salicornia probably originated during the Miocene somewhere between the Mediterranean and Central Asia from within the perennial Sarcocornia and started to diversify during Late Pliocene/Early Pleistocene. The climatic deterioration and landscape-evolution caused by orogenetic processes probably favoured the evolution and initial diversification of this annual, strongly inbreeding lineage from the perennial Sarcocornia that shows only very limited frost tolerance. The further diversification of Salicornia was promoted by at least five intercontinental dispersal events (2 x to South Africa, at least 3 x to North America) and at least two independent polyploidization events resulting in rapidly expanding tetraploid lineages, both of which are able to grow in lower belts of the saltmarshes than their diploid relatives. The diploid lineages of Salicornia also show rapid and effective range expansion resulting in both widespread genotypes and multiple genotypes in a given area. Reproductive isolation through geographical isolation after dispersal, inbreeding, and comparatively young age might be responsible for the large number of only weakly differentiated lineages. The sequence data show that the taxonomic confusion in Salicornia has two major reasons: (1) in the absence of a global revision and the presence of high phenotypic plasticity, the same widespread genotypes having been given different names in different regions, and (2) striking morphological parallelism and weak morphological differentiation led to the misapplication of the same name to different genotypes in one region.

A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.)

C4 photosynthesis is a fascinating example of parallel evolution of a complex trait involving multiple genetic, biochemical and anatomical changes. It is seen as an adaptation to deleteriously high levels of photorespiration. The current scenario for C4 evolution inferred from grasses is that it originated subsequent to the Oligocene decline in CO2 levels, is promoted in open habitats, acts as a pre-adaptation to drought resistance, and, once gained, is not subsequently lost. We test the generality of these hypotheses using a dated phylogeny of Amaranthaceae s.l. (including Chenopodiaceae), which includes the largest number of C4 lineages in eudicots. The oldest chenopod C4 lineage dates back to the Eocene/Oligocene boundary, representing one of the first origins of C4 in plants, but still corresponding with the Oligocene decline of atmospheric CO2. In contrast to grasses, the rate of transitions from C3 to C4 is highest in ancestrally drought resistant (salt-tolerant and succulent) lineages, implying that adaptation to dry or saline habitats promoted the evolution of C4; and possible reversions from C4 to C3 are apparent. We conclude that the paradigm established in grasses must be regarded as just one aspect of a more complex system of C4 evolution in plants in general.

Understanding Mediterranean-Californian disjunctions: molecular evidence from Chenopodiaceae-Betoideae

Chenopodiaceae subfam. Betoideae is distributed in both western Eurasia (four genera) and western North America (one genus). To understand the origin of this disjunction, the phylogeny of the subfamily was reconstructed and dated using ndhF, matK/trnK, tmL-trnF spacer, and ITS sequence variation, penalized likelihood and Langley-Fitch, and calibration with three different fossils. Maximum Parsimony and Maximum Likelihood analyses of the molecular data show that Betoideae are monophyletic, but that relationships of the Himalayan Acroglochin, traditionally included in Betoideae because of the shared possession of a circumscissile capsule, are uncertain. Among the betoidean genera, Beta (excl. sect. Procumbentes) is sister to a clade of Hablitzia, Patellifolia (= Beta sect. Procumbentes), Oreobliton, and Aphanisma. Apart from the strongly supported sister group relationship between the North African Oreobliton and the Califomian Aphanisma interrelationships among these four genera are not unambiguously resolved. The crown group age of Betoideae was estimated to 38.4-27.5 my using different DNA sequences, and the age of the Oreobliton/Aphanisma split to 15.4-8.1 my. Considering all evidence available, we conclude that the western Eurasian-western North American disjunction of Oreoblitom/Aphanisma is more likely to have resulted from the fragmentation of a Beringian than a North Atlantic ancestral range. Irrespective of the geographical location of this ancestral range we postulate that the evolution into dry habitats of Oreobliton and Aphanisma took place in parallel in western Eurasia and western North America. Evidence for this may be the very different life form and habitat of the two genera, of which Oreobliton is a subshrub of rocky ground at montane altitude, and Aphanisma an annual from coastal habitats. Hablitzia, a perennial vine of deciduous forests in the Caucasus area, is sister to Patellifolia/ Oreobliton/Aphanisma in the ndhF and ITS data sets. The habitat requirements of Hablitzia may be similar to those of the ancestor of the subfamily. Comparing the age of the Oreobliton/Aphanisma disjunction with ages estimated for East Asian-eastern North American disjunctions, we conclude that in many cases these two types of disjunction represent different ecological trajectories of essentially the same historical phenomenon.

A synopsis of Chenopodiaceae subfam. Betoideae and notes on the taxonomy of Beta

Abstract Kadereit, G., Hohmann, S. & Kadereit, J. W.: A synopsis of Chenopodiaceae subfam. Betoideae and notes on the taxonomy of Beta. — Willdenowia 36 (Special Issue): 9–19. — ISSN 0511-9618;

C3 and C4 leaf anatomy types in Camphorosmeae (Camphorosmoideae, Chenopodiaceae)

Complementary to our previous project on the molecular phylogeny of Camphorosmeae, the leaf anatomy of ca. 35 species including all non-Australian and selected Australian species was studied by use of light microscopy. Nine anatomical leaf types were described, compared to previous classifications, and discussed with regard to their putative evolution on the background of phylogenetic trees. Particular emphasis was given to the relationships between the C3 and C4 leaf types: Chenolea type (C3), Eokochia type (C3), Neokochia type (C3), Sedobassia type (C3/C4 intermediate), Bassia prostrata type (C4), B. muricata type (C4), B. eriantha type, B. lasiantha type (C4), Camphorosma type (C4). The main results and conclusions were: (1) Two unusual new C3 leaf types: Chenolea with microfenestrate chlorenchyma, Eokochia with unique complex vascular bundles; (2) Sedobassia interpreted as anatomically C3/C4 intermediate by kranz-like bundle sheath cells is the first C3/C4 intermediate in Camphorosmeae and found in a derived position; (3) Neokochia type detected as the likely starting point for all four C4 leaf types and for the C3/C4 intermediate; (4) hypodermis of C4 types originated from outermost chlorenchyma layer of C3 types and lost multiple times during further evolution; (5) atriplicoid Bassia. lasiantha type without water storage tissue evolved from kochioid B.muricata type; (6) two independent gains of C4 photosynthesis, one in Bassia and one in Camphorosma; (7) depending on the lineage, leaf architecture remains comparatively stable (Australian Camphorosmeae) or shows an unexpected plasticity (Bassia scoparia group).

When do different C4 leaf anatomies indicate independent C4 origins? Parallel evolution of C4 leaf types in Camphorosmeae (Chenopodiaceae)

Broad-scale phylogenetic studies give first insights in numbers, relationships, and ages of C4 lineages. They are, however, generally limited to a model that treats the evolution of the complex C4 syndrome in different lineages as a directly comparable process. Here, we use a resolved and well-sampled phylogenetic tree of Camphorosmeae, based on three chloroplast and one nuclear marker and on leaf anatomical traits to infer a more detailed picture of C4 leaf-type evolution in this lineage. Our ancestral character state reconstructions allowed two scenarios: (i) Sedobassia is a derived C3/C4 intermediate, implying two independent gains of C4 in Bassia and Camphorosma; or (ii) Sedobassia is a plesiomorphic C3/C4 intermediate, representing a syndrome ancestral to the Bassia/Camphorosma/Sedobassia lineage. In Bassia, a kochioid leaf type (Bassia muricata and/or Bassia prostrata type) is ancestral. At least three independent losses of water-storage tissue occurred, resulting in parallel shifts towards an atriplicoid leaf type. These changes in leaf anatomy are adaptations to different survival strategies in steppic or semi-desert habitats with seasonal rainfall. In contrast, Camphorosma shows a fixed C4 anatomy differing from Bassia types in its continuous Kranz layer, which indeed points to an independent origin of the full C4 syndrome in Camphorosma, either from an independent C3 or from a common C3/C4 intermediate ancestor, perhaps similar to its C3/C4 intermediate sister genus Sedobassia. The enlarged bundle sheath cells of Sedobassia might represent an important early step in C4 evolution in Camphorosmeae.

Phylogeny, biogeography and ecological diversification of Sarcocornia (Salicornioideae, Amaranthaceae).

BACKGROUND AND AIMS Sarcocornia comprises about 28 species of perennial succulent halophytes distributed worldwide, mainly in saline environments of warm-temperate and subtropical regions. The genus is characterized by strongly reduced leaves and flowers, which cause taxonomic difficulties; however, species in the genus show high diversity in growth form, with a mat-forming habit found in coastal salt marshes of all continents. Sarcocornia forms a monophyletic lineage with Salicornia whose species are all annual, yet the relationship between the two genera is poorly understood. This study is aimed at clarifying the phylogenetic relationship between Sarcocornia and Salicornia, interpreting biogeographical and ecological patterns in Sarcocornia, and gaining insights into putative parallel evolution of habit as an adaptation to environmental factors. METHODS A comprehensively sampled and dated phylogeny of Sarcocornia is presented based on nuclear ribosomal DNA (external transcribed spacer) and chloroplast DNA (atpB-rbcL, rpl32-trnL) sequences; representative samples of Salicornia were also included in the analyses. To infer biogeographical patterns, an ancestral area reconstruction was conducted. KEY RESULTS The Sarcocornia/Salicornia lineage arose during the Mid-Miocene from Eurasian ancestors and diversified into four subclades: the Salicornia clade, the American Sarcocornia clade, the Eurasian Sarcocornia clade and the South African/Australian Sarcocornia clade. Sarcocornia is supported as paraphyletic, with Salicornia nested within Sarcocornia being sister to the American/Eurasian Sarcocornia clade. The American and the South African/Australian Sarcocornia clade as well as the Salicornia clade were reconstructed to be of Eurasian origin. The prostrate, mat-forming habit arose multiple times in Sarcocornia. CONCLUSIONS Sarcocornia diversified in salt-laden environments worldwide, repeatedly evolving superficially similar prostrate, mat-forming habits that seem advantageous in stressed environments with prolonged flooding, high tidal movement and frost. Some of these prostrate-habit types might be considered as ecotypes (e.g. S. pacifica or S. pillansii) while others represent good ecospecies (e.g. S. perennis, S. decumbens, S. capensis), hence representing different stages of speciation.

Revision of Sarcocornia (Chenopodiaceae) in South Africa, Namibia and Mozambique

Abstract Sarcocornia comprises ca. 20–24 perennial, halophytic herb and shrub species. The genus is distinct from other genera in the Salicornioideae in having flowers that are more or less equal in size, arranged in a row, and with seeds that have a membranous hairy testa and lack perisperm. Sarcocornia is distributed worldwide, mainly in regions characterized by warm-temperate and, to a lesser extent, subtropical climates. The representatives of this genus are found in habitats such as estuarine salt marshes, tidal mud flats, coastal cliffs, inland salt pans, and salt-laden alluvia of intermittent semi-desert and desert streams. Some South African taxa also occur in inland (semi-desert) quartz patches while some South American species occur on saline soils of dry, continental high plateaus in the Andes. The genus reaches its highest species diversity in the Greater Cape Floristic Region of South Africa, where twelve species and one subspecies are known. This revision of southern African (South Africa, Namibia, and Mozambique) Sarcocornia comprises an identification key, the descriptions of the genus, species, and subspecies. One new combination, S. dunensis, is proposed. The former varieties recognized within S. natalensis are here treated as subspecies, S. natalensis subsp. natalensis and subsp. affinis. Morphological characters of high taxonomic value in the genus are habit (growth-form), segment morphology, and testa micromorphology. Our revision also features information on the distribution and ecology of the studied taxa.