An official website of the United States government
Summary Extant land plants consist of two deeply divergent groups, tracheophytes and bryophytes, which shared a common ancestor some 500 million years ago. While information about vascular plants and the two of the three lineages of bryophytes, the mosses and liverworts, is steadily accumulating, the biology of hornworts remains poorly explored. Yet, as the sister group to liverworts and mosses, hornworts are critical in understanding the evolution of key land plant traits. Until recently, there was no hornwort model species amenable to systematic experimental investigation, which hampered detailed insight into the molecular biology and genetics of this unique group of land plants. The emerging hornwort model species,Anthoceros agrestis, is instrumental in our efforts to better understand not only hornwort biology but also fundamental questions of land plant evolution. To this end, here we provide an overview of hornwort biology and current research on the model plantA. agrestisto highlight its potential in answering key questions of land plant biology and evolution.
more »
« less
Hornworts reveal a spatial model for pyrenoid-based CO2-concentrating mechanisms in land plants
ABSTRACT Pyrenoid-based CO2-concentrating mechanisms (pCCMs) turbocharge photosynthesis by saturating CO2around Rubisco. Hornworts are the only land plants with a pCCM. Owing to their closer relationship to crops, hornworts could offer greater translational potential compared to the green alga Chlamydomonas, the traditional model for studying pCCM. Here we report the first thorough investigation of a hornwort pCCM using the emerging modelAnthoceros agrestis. The pyrenoids inA. agrestisexhibit liquid-like properties similar to Chlamydomonas, but differ by lacking starch sheaths and being enclosed by multiple thylakoids. We found that the core pCCM components in Chlamydomonas, including BST, LCIB, and CAH3, are conserved inA. agrestisand likely have similar functions based on their subcellular localizations. Therefore, the underlying chassis for concentrating CO2might be shared between hornworts and Chlamydomonas, and ancestral to land plants. Our study presents the first spatial model for pCCM in a land plant, paving the way for future biochemical and genetic investigations.
more »
« less
- Award ID(s):
- 1923011
- PAR ID:
- 10559285
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO2to the CO2-fixing enzyme Rubisco in an organelle called the pyrenoid. Ongoing efforts seek to engineer this pyrenoid-based CO2-concentrating mechanism (PCCM) into crops to increase yields. Here we develop a computational model for a PCCM on the basis of the postulated mechanism in the green algaChlamydomonas reinhardtii. Our model recapitulates allChlamydomonasPCCM-deficient mutant phenotypes and yields general biophysical principles underlying the PCCM. We show that an effective and energetically efficient PCCM requires a physical barrier to reduce pyrenoid CO2leakage, as well as proper enzyme localization to reduce futile cycling between CO2and HCO3−. Importantly, our model demonstrates the feasibility of a purely passive CO2uptake strategy at air-level CO2, while active HCO3−uptake proves advantageous at lower CO2levels. We propose a four-step engineering path to increase the rate of CO2fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO2fixed, thereby offering a framework to guide the engineering of a PCCM into land plants.more » « less
-
Summary Despite their key phylogenetic position and their unique biology, hornworts have been widely overlooked. Until recently there was no hornwort model species amenable to systematic experimental investigation.Anthoceros agrestishas been proposed as the model species to study hornwort biology.We have developed anAgrobacterium‐mediated method for the stable transformation ofA. agrestis, a hornwort model species for which a genetic manipulation technique was not yet available.High transformation efficiency was achieved by using thallus tissue grown under low light conditions. We generated a total of 274 transgenicA. agrestislines expressing the β‐glucuronidase (GUS), cyan, green, and yellow fluorescent proteins under control of the CaMV 35S promoter and several endogenous promoters. Nuclear and plasma membrane localization with multiple color fluorescent proteins was also confirmed.The transformation technique described here should pave the way for detailed molecular and genetic studies of hornwort biology, providing much needed insight into the molecular mechanisms underlying symbiosis, carbon‐concentrating mechanism, RNA editing and land plant evolution in general.more » « less
-
Summary Recent studies have shown that correlations between chromatin modifications and transcription vary among eukaryotes. This is the case for marked differences between the chromatin of the mossPhyscomitrium patensand the liverwortMarchantia polymorpha. Mosses and liverworts diverged from hornworts, altogether forming the lineage of bryophytes that shared a common ancestor with land plants. We aimed to describe chromatin in hornworts to establish synapomorphies across bryophytes and approach a definition of the ancestral chromatin organization of land plants.We used genomic methods to define the 3D organization of chromatin and map the chromatin landscape of the model hornwortAnthoceros agrestis.We report that nearly half of the hornwort transposons were associated with facultative heterochromatin and euchromatin and formed the center of topologically associated domains delimited by protein coding genes. Transposons were scattered across autosomes, which contrasted with the dense compartments of constitutive heterochromatin surrounding the centromeres in flowering plants.Most of the features observed in hornworts are also present in liverworts or in mosses but are distinct from flowering plants. Hence, the ancestral genome of bryophytes was likely a patchwork of units of euchromatin interspersed within facultative and constitutive heterochromatin. We propose this genome organization was ancestral to land plants.more » « less
-
Abstract Hornworts are a deeply diverged lineage of bryophytes and a sister lineage to mosses and liverworts. Hornworts have an array of unique features that can be leveraged to illuminate not only the early evolution of land plants, but also alternative paths for nitrogen and carbon assimilation via cyanobacterial symbiosis and a pyrenoid-based CO2-concentrating mechanism (CCM), respectively. Despite this, hornworts are one of the few plant lineages with limited available genetic tools. Here we report an efficient biolistics method for generating transient expression and stable transgenic lines in the model hornwort, Anthoceros agrestis. An average of 569 (±268) cells showed transient expression per bombardment, with green fluorescent protein expression observed within 48–72 h. A total of 81 stably transformed lines were recovered across three separate experiments, averaging six lines per bombardment. We followed the same method to transiently transform nine additional hornwort species, and obtained stable transformants from one. This method was further used to verify the localization of Rubisco and Rubisco activase in pyrenoids, which are central proteins for CCM function. Together, our biolistics approach offers key advantages over existing methods as it enables rapid transient expression and can be applied to widely diverse hornwort species.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Posted Content:
- https://doi.org/10.1101/2024.06.26.600872
