Plant Biology Highlights: Science Articles 2017

It's almost the end of another amazing year. Undoubtedly, we came across amazing plant science stories all the year round. Like all other researchers, I regularly follow plant-specific journals (The Plant Cell, Plant Physiology, Nature Plants, The Plant Journal, Journal of Experimental Botany, Molecular Plant, Plant, Cell & Environment, Plant, Cell & Physiology, Frontiers in Plant Science, Plant Direct and so on). Apart from that Cell, Science, Nature, PNAS, Nature Communication and other renowned journals cover plant science stories. At the end of this 2017, I've covered few great stories from Science in this post. 
Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands

Soil biota influence plant performance through plant-soil feedback, but it was unclear whether the strength of such feedback depends on plant traits and whether plant-soil feedback drives local plant diversity. They grew 16 co-occurring plant species with contrasting nutrient-acquisition strategies from hyperdiverse Australian shrublands and exposed them to soil biota from under their own or other plant species. Plant responses to soil biota varied according to their nutrient-acquisition strategy, including positive feedback for ectomycorrhizal plants and negative feedback for nitrogen-fixing and nonmycorrhizal plants. Simulations revealed that such strategy-dependent feedback is sufficient to maintain the high taxonomic and functional diversity characterizing these Mediterranean-climate shrublands. This study identifies nutrient-acquisition strategy as a key trait explaining how different plant responses to soil biota promote local plant diversity. 

The root endodermis forms its extracellular diffusion barrier by developing ring-like impregnations called Casparian strips. A factor responsible for their establishment is the SCHENGEN3/GASSHO1 (SGN3/GSO1) receptor-like kinase. Its loss-of-function causes discontinuous Casparian strips. SGN3 also mediates endodermal over-lignification of other Casparian strip mutants. Yet, without ligand, SGN3 function remained elusive. Here they reported that schengen2 (sgn2) is defective in an enzyme sulfating peptide ligands. On the basis of this observation, they identified two stele-expressed peptides (CASPARIAN STRIP INTEGRITY FACTORS, CIF1/2) that complement sgn2 at nanomolar concentrations and induce Casparian strip mislocalization as well as over-lignification — all of which depend on SGN3. Direct peptide binding to recombinant SGN3 identifies these peptides as SGN3 ligands. They speculated that CIF1/2-SGN3 is part of a barrier surveillance system, evolved to guarantee effective sealing of the supracellular Casparian strip network. 

Plants achieve mineral ion homeostasis by means of a hydrophobic barrier on endodermal cells called the Casparian strip, which restricts lateral diffusion of ions between the root vascular bundles and the soil. They identified a family of sulfated peptides required for contiguous Casparian strip formation in Arabidopsis roots. These peptide hormones, which they named Casparian strip integrity factor 1 (CIF1) and CIF2, are expressed in the root stele and specifically bind the endodermis-expressed leucine-rich repeat receptor kinase GASSHO1 (GSO1)/SCHENGEN3 and its homolog, GSO2. A mutant devoid of CIF peptides is defective in ion homeostasis in the xylem. CIF genes are environmentally responsive. Casparian strip regulation is not merely a passive process driven by root developmental cues; it also serves as an active strategy to cope with adverse soil conditions. 

In plants, the perception of invading pathogens involves cell-surface immune receptor kinases. Here, they reported that the Arabidopsis SITE-1 PROTEASE (S1P) cleaves endogenous RAPID ALKALINIZATION FACTOR (RALF) propeptides to inhibit plant immunity. This inhibition is mediated by the malectin-like receptor kinase FERONIA (FER), which otherwise facilitates the ligand-induced complex formation of the immune receptor kinases EF-TU RECEPTOR (EFR) and FLAGELLIN-SENSING 2 (FLS2) with their co-receptor BRASSINOSTEROID INSENSITIVE 1–ASSOCIATED KINASE 1 (BAK1) to initiate immune signaling. They showed that FER acts as a RALF-regulated scaffold that modulates receptor kinase complex assembly. A similar scaffolding mechanism may underlie FER function in other signaling pathways. 

Modern commercial tomato varieties are substantially less flavorful than heirloom varieties. To understand and ultimately correct this deficiency, they quantified flavor-associated chemicals in 398 modern, heirloom, and wild accessions. A subset of these accessions was evaluated in consumer panels, identifying the chemicals that made the most important contributions to flavor and consumer liking. They found that modern commercial varieties contain significantly lower amounts of many of these important flavor chemicals than older varieties. Whole-genome sequencing and a genome-wide association study permitted identification of genetic loci that affect most of the target flavor chemicals, including sugars, acids, and volatiles. Together, these results provide an understanding of the flavor deficiencies in modern commercial varieties and the information necessary for the recovery of good flavor through molecular breeding. 

Plants are important in urban environments for removing pathogens and improving water quality. Seagrass meadows are the most widespread coastal ecosystem on the planet. Although these plants are known to be associated with natural biocide production, they have not been evaluated for their ability to remove microbiological contamination. Using amplicon sequencing of the 16S ribosomal RNA gene, they found that when seagrass meadows are present, there was a 50% reduction in the relative abundance of potential bacterial pathogens capable of causing disease in humans and marine organisms. Moreover, field surveys of more than 8000 reef-building corals located adjacent to seagrass meadows showed twofold reductions in disease levels compared to corals at paired sites without adjacent seagrass meadows. These results highlight the importance of seagrass ecosystems to the health of humans and other organisms.

Plants optimize carbon assimilation while limiting water loss by adjusting stomatal aperture. In grasses, a developmental innovation — the addition of subsidiary cells (SCs) flanking two dumbbell-shaped guard cells (GCs) — is linked to improved stomatal physiology. Here, they identified a transcription factor necessary and sufficient for SC formation in the wheat relative Brachypodium distachyon. Unexpectedly, the transcription factor is an ortholog of the stomatal regulator AtMUTE, which defines GC precursor fate in Arabidopsis. The novel role of BdMUTE in specifying lateral SCs appears linked to its acquisition of cell-to-cell mobility in Brachypodium. Physiological analyses on SC-less plants experimentally support classic hypotheses that SCs permit greater stomatal responsiveness and a larger range of pore apertures. Manipulation of SC formation and function in crops, therefore, may be an effective approach to enhance plant performance.

Controlling cell division plane orientation is essential for morphogenesis in multicellular organisms. In plant cells, the future cortical division plane is marked before mitotic entry by the preprophase band (PPB). Here, they characterized an Arabidopsis trm (TON1 Recruiting Motif) mutant that impairs PPB formation but does not affect interphase microtubules. Unexpectedly, PPB disruption neither abolished the capacity of root cells to define a cortical division zone nor induced aberrant cell division patterns but rather caused a loss of precision in cell division orientation. These results advocate for a reassessment of PPB function and division plane determination in plants and show that the main output of this microtubule array is to limit spindle rotations in order to increase the robustness of cell division.  

To produce seeds, flowering plants need to specify somatic cells to undergo meiosis. Here, they revealed a regulatory cascade that controls the entry into meiosis starting with a group of redundantly acting cyclin-dependent kinase (CDK) inhibitors of the KIP-RELATED PROTEIN (KRP) class. KRPs function by restricting CDKA;1 – dependent inactivation of the Arabidopsis Retinoblastoma homolog RBR1. In rbr1 and krp triple mutants, designated meiocytes undergo several mitotic divisions, resulting in the formation of supernumerary meiocytes that give rise to multiple reproductive units per future seed. One function of RBR1 is the direct repression of the stem cell factor WUSCHEL (WUS), which ectopically accumulates in meiocytes of triple krp and rbr1 mutants. Depleting WUS in rbr1 mutants restored the formation of only a single meiocyte. 

Arbuscular mycorrhizal (AM) fungi facilitate plant uptake of mineral nutrients and draw organic nutrients from the plant. Organic nutrients are thought to be supplied primarily in the form of sugars. Here, they showed that the AM fungus Rhizophagus irregularis is a fatty acid auxotroph and that fatty acids synthesized in the host plants are transferred to the fungus to sustain mycorrhizal colonization. The transfer is dependent on RAM2 (REQUIRED FOR ARBUSCULARMYCORRHIZATION 2) and the ATP binding cassette transporter – mediated plant lipid export pathway. They further showed that plant fatty acids can be transferred to the pathogenic fungus Golovinomyces cichoracerum and are required for colonization by pathogens. They suggested that the mutualistic mycorrhizal and pathogenic fungi similarly recruit the fatty acid biosynthesis program to facilitate host invasion.

Plants form beneficial associations with arbuscular mycorrhizal fungi, which facilitate nutrient acquisition from the soil. In return, the fungi receive organic carbon from the plants. The transcription factor RAM1 (REQUIRED FOR ARBUSCULAR MYCORRHIZATION 1) is crucial for this symbiosis, and they demonstrated that it is required and sufficient for the induction of a lipid biosynthetic pathway that is expressed in plant cells accommodating fungal arbuscules. Lipids are transferred from the plant to mycorrhizal fungi, which are fatty acid auxotrophs, and this lipid export requires the glycerol-3-phosphate acyltransferase RAM2, a direct target of RAM1. This work shows that in addition to sugars, lipids are a major source of organic carbon delivered to the fungus, and this is necessary for the production of fungal lipids.  

Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter 

Plants synthesize a diversity of volatile molecules that are important for reproduction and defense, serve as practical products for humans, and influence atmospheric chemistry and climate. Despite progress in deciphering plant volatile biosynthesis, their release from the cell has been poorly understood. The default assumption has been that volatiles passively diffuse out of cells. By characterization of a Petunia hybrida adenosine triphosphate–binding cassette (ABC) transporter, PhABCG1, we demonstrate that passage of volatiles across the plasma membrane relies on active transport. PhABCG1 down-regulation by RNA interference results in the decreased emission of volatiles, which accumulates to toxic levels in the plasma membrane. This study provides direct proof of a biologically mediated mechanism of volatile emission. 

Global climatic drivers of leaf size 

Leaf size varies by over a 100,000-fold among species worldwide. Although 19th-century plant geographers noted that the wet tropics harbor plants with exceptionally large leaves, the latitudinal gradient of leaf size has not been well quantified nor the key climatic drivers convincingly identified. Here, they characterized worldwide patterns in leaf size. Large-leaved species predominate in wet, hot, sunny environments; small-leaved species typify hot, sunny environments only in arid conditions; small leaves are also found in high latitudes and elevations. By modeling the balance of leaf energy inputs and outputs, we show that daytime and nighttime leaf-to-air temperature differences are key to geographic gradients in leaf size. This knowledge can enrich “next-generation” vegetation models in which leaf temperature and water use during photosynthesis play key roles. 

Distinct phases of Polycomb silencing to hold epigenetic memory of cold in Arabidopsis 

Gene silencing by Polycomb complexes is central to eukaryotic development. Cold-induced epigenetic repression of FLOWERING LOCUS C (FLC) in the plant Arabidopsis provides an opportunity to study initiation and maintenance of Polycomb silencing. Here, they showed that a subset of Polycomb repressive complex 2 factors nucleate silencing in a small region within FLC, locally increasing H3K27me3 levels. This nucleation confers a silenced state that is metastably inherited, with memory held in the local chromatin. Metastable memory is then converted to stable epigenetic silencing through separate Polycomb factors, which spread across the locus after cold to enlarge the domain that contains H3K27me3. Polycomb silencing at FLC thus has mechanistically distinct phases, which involve specialization of distinct Polycomb components to deliver first metastable then long-term epigenetic silencing.

DNA replication-coupled histone modification maintains Polycomb gene silencing in plants 

Propagation of patterns of gene expression through the cell cycle requires prompt restoration of epigenetic marks after the twofold dilution caused by DNA replication. Here, they showed that the transcriptional repressive mark H3K27me3 (histone H3 lysine 27 trimethylation) is restored in replicating plant cells through replication-coupled modification of histone variant H3.1. Plants evolved a mechanism for efficient K27 trimethylation on H3.1, which is essential for inheritance of the silencing memory from mother to daughter cells. They illustrated how this mechanism establishes H3K27me3- mediated silencing during the developmental transition to flowering. This study reveals a mechanism responsible for transmission of H3K27me3 in plant cells through cell divisions, enabling H3K27me3 to function as an epigenetic mark. 

Evolution of flower color pattern through selection on regulatory small RNAs  

Small RNAs (sRNAs) regulate genes in plants and animals. Here, they showed that population-wide differences in color patterns in snapdragon flowers are caused by an inverted duplication that generates sRNAs. The complexity and size of the transcripts indicate that the duplication represents an intermediate on the pathway to microRNA evolution. The sRNAs repress a pigment biosynthesis gene, creating a yellow highlight at the site of pollinator entry. The inverted duplication exhibits steep clines in allele frequency in a natural hybrid zone, showing that the allele is under selection. Thus, regulatory interactions of evolutionarily recent sRNAs can be acted upon by selection and contribute to the evolution of phenotypic diversity. 

Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling

In flowering plants, fertilization requires complex cell-to-cell communication events between the pollen tube and the female reproductive tissues, which are controlled by extracellular signaling molecules interacting with receptors at the pollen tube surface. They found that two such receptors in Arabidopsis, BUPS1 and BUPS2, and their peptide ligands, RALF4 and RALF19, are pollen tube–expressed and are required to maintain pollen tube integrity. BUPS1 and BUPS2 interact with receptors ANXUR1 and ANXUR2 via their ectodomains, and both sets of receptors bind RALF4 and RALF19. These receptor-ligand interactions are in competition with the female-derived ligand RALF34, which induces pollen tube bursting at nanomolar concentrations. They proposed that RALF34 replaces RALF4 and RALF19 at the interface of pollen tube–female gametophyte contact, thereby deregulating BUPS-ANXUR signaling and in turn leading to pollen tube rupture and sperm release.

RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis 

The communication of changes in the extracellular matrix to the interior of the cell is crucial for a cell’s function. The extracellular peptides of the RAPID ALKALINIZATION FACTOR (RALF) family have been identified as ligands of receptor-like kinases of the CrRLK1L subclass, but the exact mechanism of their perception is unclear. They found that Arabidopsis RALF4 and RALF19 redundantly regulate pollen tube integrity and growth and that their function depends on pollen-expressed proteins of the LEUCINE-RICH REPEAT EXTENSIN (LRX) family, which play a role in cell wall development but whose mode of action is not understood. The LRX proteins interact with RALFs, monitoring cell wall changes, which are communicated to the interior of the pollen tube via the CrRLK1L pathway to sustain normal growth. 

Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat  

Race-specific resistance genes protect the global wheat crop from stem rust disease caused by Puccinia graminis f. sp. tritici (Pgt) but are often overcome owing to the evolution of new virulent races of the pathogen. To understand virulence evolution in Pgt, they identified the protein ligand (AvrSr50) recognized by the Sr50 resistance protein. A spontaneous mutant of Pgt virulent to Sr50 contained a 2.5 mega–base pair loss-of-heterozygosity event. A haustorial secreted protein from this region triggers Sr50-dependent defense responses in planta and interacts directly with the Sr50 protein. Virulence alleles of AvrSr50 have arisen through DNA insertion and sequence divergence, and their data provide molecular evidence that in addition to sexual recombination the somatic exchange can play a role in the emergence of new virulence traits in Pgt.

If you are interested to take a look of plant biology stories from Science in 2016, please go through the following post: 


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