The remarkable plasticity of plant ontogeny is shaped by hormone pathways, which not only orchestrate intrinsic developmental programs, but also convey environmental inputs. Several classes of plant ...hormones exist, and among them auxin, brassinosteroid and gibberellin are central for the regulation of growth in general and of cell elongation in particular. Various growth phenomena can be modulated by each of the three hormones, in a sometimes synergistic fashion, suggesting physiological redundancy and/or crosstalk between the different pathways. Whether this means that they target a common and unique transcriptome module, or rather separate growth-promoting transcriptome modules, remains unclear, however. Nevertheless, while surprisingly few molecular mediators of direct crosstalk in the proper sense have been isolated, evidence is accumulating for complex cross-regulatory relations between hormone pathways at the level of transcription, as exemplified in root meristem growth. The growing number of available genome sequences from the green lineage offers first glimpses at the evolution of hormone pathways, which can aid in understanding the multiple relationships observed between these pathways in angiosperms. The available analyses suggest that auxin, gibberellin and brassinosteroid signalling arose during land plant evolution in this order, correlating with increased morphological complexity and possibly conferring increased developmental flexibility.
Phloem development Hardtke, Christian S.
The New phytologist,
August 2023, 2023-08-00, 20230801, Letnik:
239, Številka:
3
Journal Article
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Summary
The evolution of the plant vascular system is a key process in Earth history because it enabled plants to conquer land and transform the terrestrial surface. Among the vascular tissues, the ...phloem is particularly intriguing because of its complex functionality. In angiosperms, its principal components are the sieve elements, which transport phloem sap, and their neighboring companion cells. Together, they form a functional unit that sustains sap loading, transport, and unloading. The developmental trajectory of sieve elements is unique among plant cell types because it entails selective organelle degradation including enucleation. Meticulous analyses of primary, so‐called protophloem in the Arabidopsis thaliana root meristem have revealed key steps in protophloem sieve element formation at single‐cell resolution. A transcription factor cascade connects specification with differentiation and also orchestrates phloem pole patterning via noncell‐autonomous action of sieve element‐derived effectors. Reminiscent of vascular tissue patterning in secondary growth, these involve receptor kinase pathways, whose antagonists guide the progression of sieve element differentiation. Receptor kinase pathways may also safeguard phloem formation by maintaining the developmental plasticity of neighboring cell files. Our current understanding of protophloem development in the A. thaliana root has reached sufficient detail to instruct molecular‐level investigation of phloem formation in other organs.
Plants actively perceive and respond to perturbations in their cell walls which arise during growth, biotic and abiotic stresses. However, few components involved in plant cell wall integrity sensing ...have been described to date. Using a reverse-genetic approach, we identified the Arabidopsis thaliana leucine-rich repeat receptor kinase MIK2 as an important regulator of cell wall damage responses triggered upon cellulose biosynthesis inhibition. Indeed, loss-of-function mik2 alleles are strongly affected in immune marker gene expression, jasmonic acid production and lignin deposition. MIK2 has both overlapping and distinct functions with THE1, a malectin-like receptor kinase previously proposed as cell wall integrity sensor. In addition, mik2 mutant plants exhibit enhanced leftward root skewing when grown on vertical plates. Notably, natural variation in MIK2 (also named LRR-KISS) has been correlated recently to mild salt stress tolerance, which we could confirm using our insertional alleles. Strikingly, both the increased root skewing and salt stress sensitivity phenotypes observed in the mik2 mutant are dependent on THE1. Finally, we found that MIK2 is required for resistance to the fungal root pathogen Fusarium oxysporum. Together, our data identify MIK2 as a novel component in cell wall integrity sensing and suggest that MIK2 is a nexus linking cell wall integrity sensing to growth and environmental cues.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
ABSTRACT
The phloem transport network is a major evolutionary innovation that enabled plants to dominate terrestrial ecosystems. In the growth apices, the meristems, apical stem cells continuously ...produce early ‘protophloem’. This is easily observed in Arabidopsis root meristems, in which the differentiation of individual protophloem sieve element precursors into interconnected conducting sieve tubes is laid out in a spatio-temporal gradient. The mature protophloem eventually collapses as the neighboring metaphloem takes over its function further distal from the stem cell niche. Compared with protophloem, metaphloem ontogenesis is poorly characterized, primarily because its visualization is challenging. Here, we describe the improved TetSee protocol to investigate metaphloem development in Arabidopsis root tips in combination with a set of molecular markers. We found that mature metaphloem sieve elements are only observed in the late post-meristematic root, although their specification is initiated as soon as protophloem sieve elements enucleate. Moreover, unlike protophloem sieve elements, metaphloem sieve elements only differentiate once they have fully elongated. Finally, our results suggest that metaphloem differentiation is not directly controlled by protophloem-derived cues but rather follows a distinct, robust developmental trajectory.
Brassinosteroids (BRs) trigger an intracellular signaling cascade through its receptors BR INSENSITIVE 1 (BRI1), BRI1-LIKE 1 (BRL1) and BRL3. Recent studies suggest that BR-independent inputs related ...to vascular differentiation, for instance root protophloem development, modulate downstream BR signaling components. Here, we report that protophloem sieve element differentiation is indeed impaired in bri1 brl1 brl3 mutants, although this effect might not be mediated by canonical downstream BR signaling components. We also found that their small meristem size is entirely explained by reduced cell elongation, which is, however, accompanied by supernumerary formative cell divisions in the radial dimension. Thus, reduced cell expansion in conjunction with growth retardation, because of the need to accommodate supernumerary formative divisions, can account for the overall short root phenotype of BR signaling mutants. Tissue-specific re-addition of BRI1 activity partially rescued subsets of these defects through partly cell-autonomous, partly non-cell-autonomous effects. However, protophloem-specific BRI1 expression essentially rescued all major bri1 brl1 brl3 root meristem phenotypes. Our data suggest that BR perception in the protophloem is sufficient to systemically convey BR action in the root meristem context.
Soil acidification is a major agricultural problem that negatively affects crop yield 1, 2. Root systems counteract detrimental passive proton influx from acidic soil through increased proton pumping ...into the apoplast 3, which is presumably also required for cell elongation and stimulated by auxin 4, 5. Here, we found an unexpected impact of extracellular pH on auxin activity and cell proliferation rate in the root meristem of two Arabidopsis mutants with impaired auxin perception, axr3 and brx 6, 7. Surprisingly, neutral to slightly alkaline media rescued their severely reduced root (meristem) growth by stimulating auxin signaling, independent of auxin uptake. The finding that proton pumps are hyperactive in brx roots could explain this phenomenon and is consistent with more robust growth and increased fitness of brx mutants on overly acidic media or soil. Interestingly, the original brx allele was isolated from a natural stock center accession collected from acidic soil 8. Our discovery of a novel brx allele in accessions recently collected from another acidic sampling site demonstrates the existence of independently maintained brx loss-of-function alleles in nature and supports the notion that they are advantageous in acidic soil pH conditions, a finding that might be exploited for crop breeding.
► Arabidopsis BRX is essential for root meristem growth and thus root growth vigor ► Neutral extracellular pH normalizes the auxin signaling defect in brx null mutants ► Proton pump hyperactivity in brx null mutants confers adaptation to acidic soil ► This physiological feature may explain the occurrence of brx null mutants in nature
•Fundamental questions regarding phloem transport have been answered recently.•Understanding of phloem development is mostly obtained from Arabidopsis root tips.•Several genetic regulators of sieve ...element differentiation have been identified.•The toolbox to investigate sieve element differentiation has been greatly enlarged.
Evolution of the vascular tissues allowed plants to efficiently settle land, occupy new ecological niches, and thereby crucially shape earth's biosphere. Of the two conducting cell types in the plant vasculature, the tubular network of phloem sieve elements transports phloem sap from source to sink organs. Recent years have witnessed the identification of ever more regulators of sieve element differentiation, as well as a more detailed understanding of phloem physiology and function. From molecular regulators of the commitment to sieve element fate, to enzymatic executors of the differentiation process, the toolbox to investigate sieve element formation has been greatly enlarged. To connect the various players in different genetic layers, and thus to ultimately attain a comprehensive description and understanding of sieve element development at the molecular level, appears to be within reach.
Receptor kinases convey diverse environmental and developmental inputs by sensing extracellular ligands. In plants, one group of receptor‐like kinases (RLKs) is characterized by extracellular ...leucine‐rich repeat (LRR) domains, which interact with various ligands that include the plant hormone brassinosteroid and peptides of the CLAVATA3/EMBRYO SURROUNDING REGION (CLE) type. For instance, the CLE45 peptide requires the LRR‐RLK BARELY ANY MERISTEM 3 (BAM3) to prevent protophloem formation in Arabidopsis root meristems. Here, we show that other proposed CLE45 receptors, the two redundantly acting LRR‐RLKs STERILITY‐REGULATING KINASE MEMBER 1 (SKM1) and SKM2 (which perceive CLE45 in the context of pollen tube elongation), cannot substitute for BAM3 in the root. Moreover, we identify MEMBRANE‐ASSOCIATED KINASE REGULATOR 5 (MAKR5) as a post‐transcriptionally regulated amplifier of the CLE45 signal that acts downstream of BAM3. MAKR5 belongs to a small protein family whose prototypical member, BRI1 KINASE INHIBITOR 1, is an essentially negative regulator of brassinosteroid signaling. By contrast, MAKR5 is a positive effector of CLE45 signaling, revealing an unexpected diversity in the conceptual roles of MAKR genes in different signaling pathways.
Synopsis
Unlike BKI1, a negative regulator of brassinosteroid signaling, the BKI1‐related MAKR5 protein is a positive effector of CLE45 perception, revealing an unexpected diversity in the conceptual roles of MAKR genes in different signaling pathways.
SKM1 or SKM2 cannot replace BAM3 in CLE45 perception in the root.
The BKI1 and MAKR5 N‐terminal domains are interchangeable, but their C‐terminal domains are not because they are responsible for signaling pathway specificity.
MAKR5 is a positive effector of BAM3‐dependent CLE45 perception in protophloem development.
Unlike BKI1, a negative regulator of brassinosteroid signaling, the BKI1‐related MAKR5 protein is a positive effector of CLE45 perception, revealing an unexpected diversity in the conceptual roles of MAKR genes in different signaling pathways.
The root system is fundamentally important for plant growth and survival because of its role in water and nutrient uptake. Therefore, plants rely on modulation of root system architecture (RSA) to ...respond to a changing soil environment. Although RSA is a highly plastic trait and varies both between and among species, the basic root system morphology and its plasticity are controlled by inherent genetic factors. These mediate the modification of RSA, mostly at the level of root branching, in response to a suite of biotic and abiotic factors. Recent progress in the understanding of the molecular basis of these responses suggests that they largely feed through hormone homeostasis and signaling pathways. Novel factors implicated in the regulation of RSA in response to the myriad endogenous and exogenous signals are also increasingly isolated through alternative approaches such as quantitative trait locus analysis.
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