Variation in leaf anatomical traits relates to the evolution of C4 photosynthesis in Tribuloideae (Zygophyllaceae)

Lauterbach, Maximilian; Zimmer, Regina; Alexa, Andrea Christine; Adachi, Shunsuke; Sage, Rowan F.; Sage, Tammy L.; Macfarlane, Terry D.; Ludwig, Martha; Kadereit, Gudrun

doi:10.1016/j.ppees.2019.125463

Cited by 9 publications

(24 citation statements)

References 52 publications

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“…Conversely, Zygophyllaceae colonized the Atacama Desert five times independently and represents one of the very few families with truly woody representatives in this extreme habitat. Zygophyllaceae, however, entirely failed to diversify in the Atacama Desert -this is in stark contrast to the recent diversification and high species richness of Old World Zygophylloideae (Wu et al 2015, Lauterbach et al 2016 or Tribuloideae (Lauterbach et al 2019). Zygophyllaceae like most other woody genera (e.g., Balsamocarpon, Monttea, Prosopis, Skytanthus, Vasconcellea, Huidobria) only have one or very few species in the Atacama Desert, indicating a relatively low carrying capacity for this life form and/or an elevated extinction rate due to increasing aridity in the Atacama Desert (Rabosky 2013) .…”

Section: Resultsmentioning

confidence: 91%

Historical assembly of Zygophyllaceae in the Atacama Desert

Böhnert¹,

Weigend²,

Merklinger³

et al. 2020

Frontiers of Biogeography

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Section: Resultsmentioning

confidence: 91%

Historical assembly of Zygophyllaceae in the Atacama Desert

Böhnert¹,

Weigend²,

Merklinger³

et al. 2020

Frontiers of Biogeography

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“…There are multiple examples for plant lineages in which homoploid hybridization resulted in potentially adaptive genotypes through transgressive segregation, eventually leading to speciation (Gross and Rieseberg, 2005; Nieto Feliner et al, 2020). An increase of the bundle sheath to mesophyll ratio has been suggested to play an initial role in the evolution of C 4 in several plant lineages (Marshall et al, 2007; McKown and Dengler, 2007; Christin et al, 2013; Griffiths et al, 2013; Lauterbach et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Exploring the possible role of hybridization in the evolution of photosynthetic pathways in Flaveria (Asteraceae), the prime model of C₄ photosynthesis evolution

Morales‐Briones

Kadereit

2022

Preprint

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Flaveria (Asteraceae) is the prime model for the study of C4 photosynthesis evolution and seems to support a stepwise acquisition of the pathway through C3-C4 intermediate phenotypes, still existing in Flaveria today. Molecular phylogenies of Flaveria based on concatenated data matrices are currently used to reconstruct the complex sequence of trait shifts during C4 evolution. To assess the possible role of hybridization in C4 evolution in Flaveria, we re-analyzed transcriptome data of 17 Flaveria species to infer the extent of gene tree discordance and possible reticulation events. We found massive gene tree discordance as well as reticulation along the backbone and within clades containing C3-C4 intermediate and C4-like species. An early hybridization event between two C3 species might have triggered C4 evolution in the genus. The clade containing all C4 species plus the C4-like species F. vaginata and F. palmeri is robust but of hybrid origin involving F. angustifolia and F. sonorensis (both C3-C4 intermediate) as parental lineages. Hybridization seems to be a driver of C4 evolution in Flaveria and likely promoted the fast acquisition of C4 traits. This new insight can be used in further exploring C4 evolution and can inform C4 bioengineering efforts.

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“…The structural characteristics observed here are consistent with patterns in other C 4 clades. NADP-ME species among C 4 grasses, sedges and eudicots (as shown in Flaveria, Euphorbia, Gomphrena, Heliotropium, Salsola, and Tribulus) share with Boerhavia and Portulaca pilosa the pattern of enlarged chloroplasts with weakly developed grana stacks, and few BS mitochondria (Carolin et al, 1978;Kim and Fisher, 1990;Ueno, 1996Ueno, , 2013Voznesenskaya et al, 1999;Yoshimura et al, 2004;Muhaidat et al, 2011;Sage T. L. et al, 2011;Lauterbach et al, 2019). NAD-ME eudicots in Amaranthus, Atriplex, Anticharis, Cleome, Gisekia, Salsola, Suaeda, and Tecticornia share with Allionia and P. oleracea the pattern of enlarged chloroplasts with well-developed grana and large numbers of interspersed mitochondria (Carolin et al, 1978;Voznesenskaya et al, 1999Voznesenskaya et al, , 2007Voznesenskaya et al, , 2008Khoshravesh et al, 2012;Bissinger et al, 2014;Oakley et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…With sequencing data becoming widely available, it may be possible to identify C 4 -subtypes using transcriptomics (Lauterbach et al, 2019). Such an approach, however, could produce errors if not coupled with enzyme activity assays.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Convergence of C4 Photosynthesis: A Case Study in the Nyctaginaceae

et al. 2020

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C 4 photosynthesis evolved over 65 times, with around 24 origins in the eudicot order Caryophyllales. In the Caryophyllales family Nyctaginaceae, the C 4 pathway is known in three genera of the tribe Nyctagineae: Allionia, Okenia and Boerhavia. Phylogenetically, Allionia and Boerhavia/Okenia are separated by three genera whose photosynthetic pathway is uncertain. To clarify the distribution of photosynthetic pathways in the Nyctaginaceae, we surveyed carbon isotope ratios of 159 species of the Nyctaginaceae, along with bundle sheath (BS) cell ultrastructure, leaf gas exchange, and C 4 pathway biochemistry in five species from the two C 4 clades and closely related C 3 genera. All species in Allionia, Okenia and Boerhavia are C 4 , while no C 4 species occur in any other genera of the family, including three that branch between Allionia and Boerhavia. This demonstrates that C 4 photosynthesis evolved twice in Nyctaginaceae. Boerhavia species use the NADP-malic enzyme (NADP-ME) subtype of C 4 photosynthesis, while Allionia species use the NAD-malic enzyme (NAD-ME) subtype. The BS cells of Allionia have many more mitochondria than the BS of Boerhavia. Bundle sheath mitochondria are closely associated with chloroplasts in Allionia which facilitates CO 2 refixation following decarboxylation by mitochondrial NAD-ME. The close relationship between Allionia and Boerhavia could provide insights into why NADP-ME versus NAD-ME subtypes evolve, particularly when coupled to analysis of their respective genomes. As such, the group is an excellent system to dissect the organizational hierarchy of convergent versus divergent traits produced by C 4 evolution, enabling us to understand when convergence is favored versus when divergent modifications can result in a common phenotype.

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Variation in leaf anatomical traits relates to the evolution of C4 photosynthesis in Tribuloideae (Zygophyllaceae)

Cited by 9 publications

References 52 publications

Historical assembly of Zygophyllaceae in the Atacama Desert

Historical assembly of Zygophyllaceae in the Atacama Desert

Exploring the possible role of hybridization in the evolution of photosynthetic pathways in Flaveria (Asteraceae), the prime model of C₄ photosynthesis evolution

Evolutionary Convergence of C4 Photosynthesis: A Case Study in the Nyctaginaceae

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Variation in leaf anatomical traits relates to the evolution of C4 photosynthesis in Tribuloideae (Zygophyllaceae)

Cited by 9 publications

References 52 publications

Historical assembly of Zygophyllaceae in the Atacama Desert

Historical assembly of Zygophyllaceae in the Atacama Desert

Exploring the possible role of hybridization in the evolution of photosynthetic pathways in Flaveria (Asteraceae), the prime model of C4 photosynthesis evolution

Evolutionary Convergence of C4 Photosynthesis: A Case Study in the Nyctaginaceae

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Exploring the possible role of hybridization in the evolution of photosynthetic pathways in Flaveria (Asteraceae), the prime model of C₄ photosynthesis evolution