Yin Long Qiu

Phylogenetic distribution and evolution of mycorrhizas in land plants

A survey of 659 papers mostly published since 1987 was conducted to compile a checklist of mycorrhizal occurrence among 3,617 species (263 families) of land plants. A plant phylogeny was then used to map the mycorrhizal information to examine evolutionary patterns. Several findings from this survey enhance our understanding of the roles of mycorrhizas in the origin and subsequent diversification of land plants. First, 80 and 92% of surveyed land plant species and families are mycorrhizal. Second, arbuscular mycorrhiza (AM) is the predominant and ancestral type of mycorrhiza in land plants. Its occurrence in a vast majority of land plants and early-diverging lineages of liverworts suggests that the origin of AM probably coincided with the origin of land plants. Third, ectomycorrhiza (ECM) and its derived types independently evolved from AM many times through parallel evolution. Coevolution between plant and fungal partners in ECM and its derived types has probably contributed to diversification of both plant hosts and fungal symbionts. Fourth, mycoheterotrophy and loss of the mycorrhizal condition also evolved many times independently in land plants through parallel evolution.

The deepest divergences in land plants inferred from phylogenomic evidence.

Phylogenetic relationships among the four major lineages of land plants (liverworts, mosses, hornworts, and vascular plants) remain vigorously contested; their resolution is essential to our understanding of the origin and early evolution of land plants. We analyzed three different complementary data sets: a multigene supermatrix, a genomic structural character matrix, and a chloroplast genome sequence matrix, using maximum likelihood, maximum parsimony, and compatibility methods. Analyses of all three data sets strongly supported liverworts as the sister to all other land plants, and analyses of the multigene and chloroplast genome matrices provided moderate to strong support for hornworts as the sister to vascular plants. These results highlight the important roles of liverworts and hornworts in two major events of plant evolution: the water-to-land transition and the change from a haploid gametophyte generation-dominant life cycle in bryophytes to a diploid sporophyte generation-dominant life cycle in vascular plants. This study also demonstrates the importance of using a multifaceted approach to resolve difficult nodes in the tree of life. In particular, it is shown here that densely sampled taxon trees built with multiple genes provide an indispensable test of taxon-sparse trees inferred from genome sequences.

Angiosperm phylogeny: 17 genes, 640 taxa

PREMISE OF THE STUDY Recent analyses employing up to five genes have provided numerous insights into angiosperm phylogeny, but many relationships have remained unresolved or poorly supported. In the hope of improving our understanding of angiosperm phylogeny, we expanded sampling of taxa and genes beyond previous analyses. METHODS We conducted two primary analyses based on 640 species representing 330 families. The first included 25260 aligned base pairs (bp) from 17 genes (representing all three plant genomes, i.e., nucleus, plastid, and mitochondrion). The second included 19846 aligned bp from 13 genes (representing only the nucleus and plastid). KEY RESULTS Many important questions of deep-level relationships in the nonmonocot angiosperms have now been resolved with strong support. Amborellaceae, Nymphaeales, and Austrobaileyales are successive sisters to the remaining angiosperms (Mesangiospermae), which are resolved into Chloranthales + Magnoliidae as sister to Monocotyledoneae + [Ceratophyllaceae + Eudicotyledoneae]. Eudicotyledoneae contains a basal grade subtending Gunneridae. Within Gunneridae, Gunnerales are sister to the remainder (Pentapetalae), which comprises (1) Superrosidae, consisting of Rosidae (including Vitaceae) and Saxifragales; and (2) Superasteridae, comprising Berberidopsidales, Santalales, Caryophyllales, Asteridae, and, based on this study, Dilleniaceae (although other recent analyses disagree with this placement). Within the major subclades of Pentapetalae, most deep-level relationships are resolved with strong support. CONCLUSIONS Our analyses confirm that with large amounts of sequence data, most deep-level relationships within the angiosperms can be resolved. We anticipate that this well-resolved angiosperm tree will be of broad utility for many areas of biology, including physiology, ecology, paleobiology, and genomics.

Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution

To study the tempo and pattern of mitochondrial gene loss in plants, DNAs from 280 genera of flowering plants were surveyed for the presence or absence of 40 mitochondrial protein genes by Southern blot hybridization. All 14 ribosomal protein genes and both sdh genes have been lost from the mitochondrial genome many times (6 to 42) during angiosperm evolution, whereas only two losses were detected among the other 24 genes. The gene losses have a very patchy phylogenetic distribution, with periods of stasis followed by bursts of loss in certain lineages. Most of the oldest groups of angiosperms are still mired in a prolonged stasis in mitochondrial gene content, containing nearly the same set of genes as their algal ancestors more than a billion years ago. In sharp contrast, other plants have rapidly lost many or all of their 16 mitochondrial ribosomal protein and sdh genes, thereby converging on a reduced gene content more like that of an animal or fungus than a typical plant. In these and many lineages with more modest numbers of losses, the rate of ribosomal protein and sdh gene loss exceeds, sometimes greatly, the rate of mitochondrial synonymous substitutions. Most of these mitochondrial gene losses are probably the consequence of gene transfer to the nucleus; thus, rates of functional gene transfer also may vary dramatically in angiosperms.

Molecular phylogenetics of the Magnoliidae: cladistic analyses of nucleotide sequences of the plastid gene rbcL

Nucleotide sequences of the plastid protein-coding gene rbcL from 64 species of 36 families in subclass Magnoliidae sensu Cronquist and representatives of all other major seed plant groups were analyzed by parsimony in a series of four analyses. Ceratophyllum (Ceratophyllaceae) was found to be sister to all other angiosperms. Other magnoliids formed five major groups, roughly corresponding to the Magnoliales, Laurales, Aristolochiaceae/Piperales, Nymphaeales, and Ranunculales/Papaverales. Four magnoliid lineages, those with monosulcate or monosulcate-derived pollen (Magnoliales, Laurales, Aristolochiales/Piperales, and Nymphaeales), and the monocots (with the same type of pollen) formed a weakly supported monophyletic group

A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes

Nucleotide sequences of seven chloroplast (atpB and rbcL, SSU and LSU rDNAs), mitochondrial (atp1, LSU rDNA), and nuclear (18S rDNA) genes from 192 land plants and their algal relatives were analyzed using maximum likelihood and maximum parsimony methods. Liverworts, mosses, hornworts, lycophytes, monilophytes (ferns), seed plants, and angiosperms all represent strongly supported monophyletic groups. Three bryophyte lineages form a paraphyletic group to vascular plants, with liverworts representing the sister to all other land plants and hornworts being sister to vascular plants. Lycophytes are sister to all other vascular plants, which are divided into two clades, one being monilophytes, which include Equisetum, Psilotaceae‐Ophioglossaceae, Marattiaceae, and leptosporangiate ferns, and the other being seed plants. Relationships among the monilophyte lineages remain unresolved. Within seed plants, extant gymnosperms form a moderately supported clade in which Gnetales are related to conifers. This clade is sister to angiosperms. Most of the relationships among all major lineages of nonflowering land plants are supported by bootstrap values of 75% or higher, except those among basal monilophyte lineages and among some gymnosperm lineages, probably because of extinctions. The closest algal relative of land plants is Characeae, and this relationship is well supported. Several methodological issues on reconstructing large, deep phylogenies are also discussed.

Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants.

*The colonization of land by plants fundamentally altered environmental conditions on earth. Plant-mycorrhizal fungus symbiosis likely played a key role in this process by assisting plants to absorb water and nutrients from soil. *Here, in a diverse set of land plants, we investigated the evolutionary histories and functional conservation of three genes required for mycorrhiza formation in legumes and rice (Oryza sativa), DMI1, DMI3 and IPD3. *The genes were isolated from nearly all major plant lineages. Phylogenetic analyses showed that they had been vertically inherited since the origin of land plants. Further, cross-species mutant rescue experiments demonstrated that DMI3 genes from liverworts and hornworts could rescue Medicago truncatula dmi3 mutants for mycorrhiza formation. Yeast two-hybrid assays also showed that bryophyte DMI3 proteins could bind to downstream-acting M. trunculata IPD3 protein. Finally, molecular evolutionary analyses revealed that these genes were under purifying selection for maintenance of their ancestral functions in all mycorrhizal plant lineages. *These results indicate that the mycorrhizal genes were present in the common ancestor of land plants, and that their functions were largely conserved during land plant evolution. The evidence presented here strongly suggests that plant-mycorrhizal fungus symbiosis was one of the key processes that contributed to the origin of land flora.

Phylogenetic Analyses of Basal Angiosperms Based on Nine Plastid, Mitochondrial, and Nuclear Genes

DNA sequences of nine genes (plastid: atpB, matK, and rbcL; mitochondrial: atp1, matR, mtSSU, and mtLSU; nuclear: 18S and 26S rDNAs) from 100 species of basal angiosperms and gymnosperms were analyzed using parsimony, Bayesian, and maximum likelihood methods. All of these analyses support the following consensus of relationships among basal angiosperms. First, Amborella, Nymphaeaceae, and Austrobaileyales are strongly supported as a basal grade in the angiosperm phylogeny, with either Amborella or Amborella and Nymphaeales as sister to all other angiosperms. An examination of nucleotide substitution patterns of all nine genes ruled out any possibility of analytical artifacts because of RNA editing and GC‐content bias in placing these taxa at the base of the angiosperm phylogeny. Second, Magnoliales are sister to Laurales and Piperales are sister to Canellales. These four orders together constitute the magnoliid clade. Finally, the relationships among Ceratophyllum, Chloranthaceae, monocots, magnoliids, and eudicots are resolved in different ways in various analyses, mostly with low support. Our study indicates caution in total evidence approaches in that some of the genes employed (e.g., mtSSU, mtLSU, and nuclear 26S rDNA) added signal that conflicted with the other genes in resolving certain parts of the phylogenetic tree.

Phylogenetic analyses and perianth evolution in basal angiosperms

Using a compartmentalization approach, we conducted phylogenetic analyses of the basalmost extant angiosperms using sequences from six genes (over 12,000 bp per taxon) from all three genomes (chloroplast-atpB, rbcL; nuclear- 18S rDNA, 26S rDNA; mitochondrial-matR, atpA). Trees resulting from parsimony and maximum likelihood analyses of the compartmentalized data are identical. We find strong support (100% for each node) for the earliest-branching angiosperms: Amborellaceae, Nymphaeaceae, and an Austrobaileyales clade (Illiciaceae, Schisandraceae, Trimeniaceae, Austrobaileyaceae). Whereas most recent studies using multiple genes provided poor resolution and support for relationships among the remaining basal angiosperms (Ceratophyllaceae, Chloranthaceae, Canellales ( = Winterales), Piperales, monocots, Magnoliales, Laurales), with compartmentalization, we find high levels (> 90%) of bootstrap support for relationships among these clades. Canellales and Piperales form a strongly supported (100%) sister group that is, in turn, sister to a well-supported (100%) clade of Laurales and Magnoliales. Canellales + Piperales and Magnoliales + Laurales form a well-supported magnoliid clade. Ceratophyllaceae are strongly supported (100%) as sister to the monocots; the monocot/Ceratophyllaceae clade is well supported (86%) as sister to all remaining angiosperms (Chloranthaceae, the magnoliid clade, and eudicots). The addition of entire 26S rDNA sequences clearly contributed to this increased internal support. We examined the diversification of perianth phyllotaxis, merosity, and differentiation using our phylogenetic hypothesis for angiosperms. Ancestral perianth phyllotaxis and merosity are equivocal for each node of the Amborellaceae, Nymphaeaceae, Austrobaileyales grade; however, an undifferentiated perianth is reconstructed as the ancestral state for the angiosperms. Trimery and whorled perianth phyllotaxis have played a major role in basal angiosperm perianth evolution and represent the ancestral states for the large Glade comprising all angiosperms other than Amborella, Nymphaeaceae, and Austrobaileyales. A differentiated perianth has apparently evolved multiple times.

Angiosperm phylogeny inferred from sequences of four mitochondrial genes

Abstract  An angiosperm phylogeny was reconstructed in a maximum likelihood analysis of sequences of four mitochondrial genes, atp1, matR, nad5, and rps3, from 380 species that represent 376 genera and 296 families of seed plants. It is largely congruent with the phylogeny of angiosperms reconstructed from chloroplast genes atpB, matK, and rbcL, and nuclear 18S rDNA. The basalmost lineage consists of Amborella and Nymphaeales (including Hydatellaceae). Austrobaileyales follow this clade and are sister to the mesangiosperms, which include Chloranthaceae, Ceratophyllum, magnoliids, monocots, and eudicots. With the exception of Chloranthaceae being sister to Ceratophyllum, relationships among these five lineages are not well supported. In eudicots, Ranunculales, Sabiales, Proteales, Trochodendrales, Buxales, Gunnerales, Saxifragales, Vitales, Berberidopsidales, and Dilleniales form a basal grade of lines that diverged before the diversification of rosids and asterids. Within rosids, the COM (Celastrales–Oxalidales–Malpighiales) clade is sister to malvids (or rosid II), instead of to the nitrogen‐fixing clade as found in all previous large‐scale molecular analyses of angiosperms. Santalales and Caryophyllales are members of an expanded asterid clade. This study shows that the mitochondrial genes are informative markers for resolving relationships among genera, families, or higher rank taxa across angiosperms. The low substitution rates and low homoplasy levels of the mitochondrial genes relative to the chloroplast genes, as found in this study, make them particularly useful for reconstructing ancient phylogenetic relationships. A mitochondrial gene‐based angiosperm phylogeny provides an independent and essential reference for comparison with hypotheses of angiosperm phylogeny based on chloroplast genes, nuclear genes, and non‐molecular data to reconstruct the underlying organismal phylogeny.