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Transition from C3 to proto-Kranz to C3-C4 intermediate type in the genus Chenopodium (Chenopodiaceae).

ABSTRACT: The Chenopodiaceae is one of the families including C4 species among eudicots. In this family, the genus Chenopodium is considered to include only C3 species. However, we report here a transition from C3 photosynthesis to proto-Kranz to C3-C4 intermediate type in Chenopodium. We investigated leaf anatomical and photosynthetic traits of 15 species, of which 8 species showed non-Kranz anatomy and a CO2 compensation point (?) typical of C3 plants. However, 5 species showed proto-Kranz anatomy and a C3-like ?, whereas C. strictum showed leaf anatomy and a ? typical of C3-C4 intermediates. Chenopodium album accessions examined included both proto-Kranz and C3-C4 intermediate types, depending on locality. Glycine decarboxylase, a key photorespiratory enzyme that is involved in the decarboxylation of glycine, was located predominantly in the mesophyll (M) cells of C3 species, in both M and bundle-sheath (BS) cells in proto-Kranz species, and exclusively in BS cells in C3-C4 intermediate species. The M/BS tissue area ratio, number of chloroplasts and mitochondria per BS cell, distribution of these organelles to the centripetal region of BS cells, the degree of inner positioning (vacuolar side of chloroplasts) of mitochondria in M cells, and the size of BS mitochondria also changed with the change in glycine decarboxylase localization. All Chenopodium species examined were C3-like regarding activities and amounts of C3 and C4 photosynthetic enzymes and ?13C values, suggesting that these species perform photosynthesis without contribution of the C4 cycle. This study demonstrates that Chenopodium is not a C3 genus and is valuable for studying evolution of C3-C4 intermediates.

SUBMITTER: Yorimitsu Y

PROVIDER: S-EPMC7205854 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Transition from C3 to proto-Kranz to C3-C4 intermediate type in the genus Chenopodium (Chenopodiaceae).

Yorimitsu Yuki Y Kadosono Aya A Hatakeyama Yuto Y Yabiku Takayuki T Ueno Osamu O

Journal of plant research 20190831 6

The Chenopodiaceae is one of the families including C4 species among eudicots. In this family, the genus Chenopodium is considered to include only C3 species. However, we report here a transition from C3 photosynthesis to proto-Kranz to C3-C4 intermediate type in Chenopodium. We investigated leaf anatomical and photosynthetic traits of 15 species, of which 8 species showed non-Kranz anatomy and a CO2 compensation point (Γ) typical ...[more]

PMID: 31473860

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Project description:BackgroundChloroplast genome information is critical to understanding forms of photosynthesis in the plant kingdom. During the evolutionary process, plants have developed different photosynthetic strategies that are accompanied by complementary biochemical and anatomical features. Members of family Chenopodiaceae have species with C3 photosynthesis, and variations of C4 photosynthesis in which photorespiration is reduced by concentrating CO2 around Rubisco through dual coordinated functioning of dimorphic chloroplasts. Among dicots, the family has the largest number of C4 species, and greatest structural and biochemical diversity in forms of C4 including the canonical dual-cell Kranz anatomy, and the recently identified single cell C4 with the presence of dimorphic chloroplasts separated by a vacuole. This is the first comparative analysis of chloroplast genomes in species representative of photosynthetic types in the family.ResultsMethodology with high throughput sequencing complemented with Sanger sequencing of selected loci provided high quality and complete chloroplast genomes of seven species in the family and one species in the closely related Amaranthaceae family, representing C3, Kranz type C4 and single cell C4 (SSC4) photosynthesis six of the eight chloroplast genomes are new, while two are improved versions of previously published genomes. The depth of coverage obtained using high-throughput sequencing complemented with targeted resequencing of certain loci enabled superior resolution of the border junctions, directionality and repeat region sequences. Comparison of the chloroplast genomes with previously sequenced plastid genomes revealed similar genome organization, gene order and content with a few revisions. High-quality complete chloroplast genome sequences resulted in correcting the orientation the LSC region of the published Bienertia sinuspersici chloroplast genome, identification of stop codons in the rpl23 gene in B. sinuspersici and B. cycloptera, and identifying an instance of IR expansion in the Haloxylon ammodendron inverted repeat sequence. The rare observation of a mitochondria-to-chloroplast inter-organellar gene transfer event was identified in family Chenopodiaceae.ConclusionsThis study reports complete chloroplast genomes from seven Chenopodiaceae and one Amaranthaceae species. The depth of coverage obtained using high-throughput sequencing complemented with targeted resequencing of certain loci enabled superior resolution of the border junctions, directionality, and repeat region sequences. Therefore, the use of high throughput and Sanger sequencing, in a hybrid method, reaffirms to be rapid, efficient, and reliable for chloroplast genome sequencing.

Project description:AimUsing the extremophile genus Anabasis, which includes c. 28 succulent, xerophytic C4 species, and is widely distributed in arid regions of Northern Africa, Arabia, and Asia, we investigate biogeographical relationships between the Irano-Turanian floristic region (ITfr) and its neighboring regions. We test whether the spread of arid and semi-arid biomes in Eurasia coincides with the biogeography of this drought-adapted genus, and whether the ITfr acted as source area of floristic elements for adjacent regions.LocationDeserts and semi-deserts of Northern Africa, Mediterranean, Arabia, West and Central Asia.MethodsFour cpDNA markers (rpL16 intron, atpB-rbcL, trnQ-rps16, and ndhF-rpL32 spacers) were sequenced for 58 accessions representing 21 Anabasis species. Phylogenetic relationships and divergence times were inferred using maximum likelihood and a time-calibrated Bayesian approach. To document the extant distribution of Anabasis, material from 23 herbaria was surveyed resulting in 441 well-documented collections used for the coding of eight floristic regions. Using this coded data, ancestral range was estimated using "BioGeoBEARS" under the DEC model.ResultsAnabasis originated during the Late Miocene and the ancestral range was probably widespread and disjunct between Western Mediterranean and the Irano-Turanian regions. Diversification started with two divergence events at the Miocene/Pliocene boundary (5.1 and 4.5 mya) leading to Asian clade I with ITfr origin which is sister to a slightly younger Asian clade II, which originated in the Western ITfr, and a Mediterranean/North African clade with an origin in the Western Mediterranean.Main conclusionsAnabasis did not follow aridification and continuously expanded its distribution area, in fact its probably wide ancestral distribution area seems to have been fragmented during the very Late Miocene and the remnant lineages then expanded into neighboring arid regions. This genus supports the role of the ITfr as source area for xerophytic elements in the Mediterranean and Central Asia.

Dataset Information

Transition from C3 to proto-Kranz to C3-C4 intermediate type in the genus Chenopodium (Chenopodiaceae).

Publications

Transition from C<sub>3</sub> to proto-Kranz to C<sub>3</sub>-C<sub>4</sub> intermediate type in the genus Chenopodium (Chenopodiaceae).

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