Angiosperm Evolution
In previous posts I have briefly mentioned that angiosperms (flowering plants) evolved sometime between 140 and 200 million years ago (see C4 Photosynthesis, Light Reactions of Photosynthesis). Here I would like to get into a little more detail on this subject.
Cyanobacteria likely evolved over 3 billion years ago and "invented" the process of photosynthesis, splitting water, and creating oxygen. Initially this oxygen simply reacted with iron in the oceans, forming iron oxides (rust) that precipitated out of solution (Hohmann-Marriott and Blankenship (2011)). Eventually, however, this oxygen began to build up in the atmosphere, allowing for the evolution of the first primitive eukaryotic cells with nucleus and mitochondrion that likely fed on cyanobacteria as a primary food source. Approximately 1.2 billion years ago one such eukaryotic cell ingested a cyanobacterium but instead of digesting it, retained it, with the cyanobacterium becoming the chloroplast. This single endosymbiotic event, leading to the first photosynthetic eukaryotes (with chloroplast, mitochondrion and nucleus), gave rise to the entire plant lineage. Initially this organism and its progeny would have been unicellular green algae (phytoplankton). Somehow they survived "snowball earth" when the earth's surface became almost entirely frozen, approximately 580–850 million years ago (Snowball Earth - Wikipedia).
Emerging from "snowball earth" (the Cryogenian) were the first multicellular algae. These organisms further enhanced oxygen levels in the atmosphere, and permitted evolution of multicellular animals relying on oxygen and plant carbohydrates as energy sources (Hohmann-Marriott and Blankenship (2011)). This oxygenation of the atmosphere led to the Cambrian explosion (beginning about 540 million years ago) when most major animal phyla appeared in the fossil record (Cambrian explosion - Wikipedia).
Plants did not make the transition to land until about 600 million years ago in the form of mosses, which evolved further into liverworts, lycophytes and eventually ferns and progymnosperms by about 400 million years ago. The progymnosperms then evolved into pines, Ginkgos and cycads by about 350 million years ago. These transitions were not trivial and entailed development of well-developed roots, vascular tissues, lignified cell walls, and stomata, and specialized reproductive organs and seeds (see The seed biology place for further details).
Origin and evolution of the seed habit. Image Source:
The rapid diversification of these organisms resulted in huge deposits of plant material on land during the carboniferous period that we now harvest as coal.
The End-Permian extinction event (the great dying or the Permian–Triassic extinction event - Wikipedia) at around 250 million years ago caused a number of extinctions of these organisms, but land plant survivors included mosses, liverworts, ferns, pines, Ginkgos and cycads. The End-Permian extinction event is thought to have been caused by massive volcanic eruptions in the Siberian traps region. It is further postulated that this volcanism seeded the atmosphere and oceans with nickel which then triggered massive release of toxic methane from the oceans. The presumed culprit was an ocean dwelling bacterium that had evolved a nickel-dependent enzyme for converting acetate to methane (Rothman et al. (2014))!
It is thought that angiosperms (flowering plants) may first have evolved in the aftermath of this End-Permian extinction event although they did not begin to establish a strong foothold until approximately 140 million years ago. It is postulated that the earliest angiosperms may have survived in isolated refugia for about 100 million years (throughout the Triassic and Jurassic periods) before their rapid explosion in diversity during the Cretaceous period. Charles Darwin referred to this rapid explosion of angiosperms as 'an abominable mystery' (Friedman (2009)).
Angiosperm seed evolution and species diversification: Darwin's abominable mystery. Image Source:
The principal distinguishing characteristics of the angiosperm lineage are: flowers, covered seeds, and a triploid endosperm (cf. gymnosperms with naked seed and haploid endosperm). Angiosperms also possess a more complex lignin than gymnosperms (Weng and Chapple, 2010).
It is noteworthy that dinosaurs came into prominence after the End-Permian extinction event and survived until approximately 66 million years ago; thus, angiosperms and dinosaurs co-existed. The large herbivorous dinosaurs probably transitioned from a diet of mainly gymnosperms, ferns and fern allies as food sources during the Jurassic period, to a diet enriched in angiosperms by the late Cretaceous (Hummel et al. (2008)).
A major impact event releases the energy of several million nuclear weapons detonating simultaneously, when an asteroid of only a few kilometers in diameter collides with a larger body such as the Earth (image: artist's impression). Image Source:
Although the most widely accepted hypothesis is that dinosaurs became extinct 66 million years ago as a result of an asteroid impact (the Chicxulub asteroid impact event), it has been suggested that Deccan traps volcanism also played a role (Cretaceous–Paleogene extinction event - Wikipedia). It has also been further postulated that angiosperms may have contributed to the demise of non-avian dinosaurs (see Frederick and Gallup (2017) and references cited therein). Many angiosperms (including members of the Asteraceae) are known to accumulate toxic alkaloids such as pyrrolizidine alkaloids which could have been poisonous to large herbivores (Castells et al. (2014)). Early members of the Asteraceae appeared about 80 million years ago (Barreda et al. (2015)). However, analyses of plant and dinosaur diversity do not reveal any strong correlations, perhaps with the single exception of Stegosauria (Butler et al. (2009)). Stegosaurs likely fed on cycads and were thought to be dispersers of cycad seeds. With the rise of angiosperms, overtaking environmental niches formerly occupied by cycads, a decline of cycads may have contributed to stegosaur decline prior to the Cretaceous-Tertiary (K-T) or Cretaceous-Paleogene (K-Pg) extinction event (Butler et al. (2009)). According to Barrett (2014) ... "Although dinosaur herbivores lived through several major events in floral evolution, there is currently no evidence for plant-dinosaur coevolutionary interactions."
Angiosperms did survive this extinction event most likely because of their dormant seeds. Nevertheless, there were massive initial disruptions of the North American vegetation as a result of this extinction event, followed by slow recovery after a spike of ferns which are typically the first to colonize "disturbed areas". In North America, it is estimated that approximately 57% of plant species became extinct (Chaloner (2009), Cretaceous–Paleogene extinction event - Wikipedia). Interestingly, a number of whole-genome duplications (WGDs) have been discovered to have occurred during angiosperm evolution, and these seem to coincide with mass extinction events. A number of WGDs occurred simultaneously in various angiosperm families shortly after the Cretaceous-Tertiary (K-T) or Cretaceous-Paleogene (K-Pg) extinction event (Fawcett et al. (2009), Jiao et al. (2011)), and this was preceded by a WGD around 140 million years ago at the Jurassic-Cretaceous boundary (Jiao et al. (2011)). The burst of WGDs following the K-Pg extinction may have permitted angiosperms to exploit new environmental niches. With extra copies of all genes, plants with WGDs could readily modify these duplicated genes to perform new functions without impairing the functions of the original copies (Fawcett et al. (2009), Soltis and Soltis (2016)).
The flowering plant Amborella trichopoda appears to be the sole survivor of ancient, basal angiosperms and is recognized as "the single living species of the sister lineage to all other extant flowering plants". Both the nuclear (Amborella Genome Project (2013)) and chloroplast (Gitzendanner et al. (2018)) genomes of Amborella have been sequenced and these accomplishments have been critically important in elucidating angiosperm genome diversification and duplication.
I encourage readers to explore the Tree of Life Web Project: Angiosperms (Flowering Plants) to learn more about angiosperm evolution and the importance of Amborella trichopoda at the root of this tree.
References
Chaloner, B. Plants and the K–T Boundary. Annals of Botany 103: v–vi (2009)
Friedman, W.E. The meaning of Darwin's 'abominable mystery'. Am. J. Bot. 96: 5-21 (2009)
Please feel free to comment or ask questions below. I will try to answer as soon as possible.
He had a Ginkgo tree at our institute. Unfortunately, it was the female tree that made an incredible amount of fruits every autumn. For non-plant people: it smells like a very stinky cheese.
Thank you for the link to ToL Project
Yes, they are very smelly. I think that there is only one Ginkgo species left (biloba), which somehow managed to survive the end Permian and the dinosaur killing asteroid impact!
Tardigrades of plant world :)
Very educational thanks.
Thank you!