Differential gene expression and transport functionality in the bundle sheath versus mesophyll – a potential role in leaf mineral homeostasis

Wigoda, Noa; Pasmanik‐Chor, Metsada; Yang, Ting; Yu, Ling; Moshelion, Menachem; Moran, Nava

doi:10.1093/jxb/erx067

Cited by 22 publications

(72 citation statements)

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“…This strengthens the idea that BS cells are a point of control for the radial transport of solutes. The transcriptomic data also indicate that AtLYK5 is expressed at detectable levels in both BS and mesophyll cells, as seen in the normalized log 2 data (intensity value) 38 . To act as a checkpoint for the movement of any substance into the mesophyll cells from the vascular tissues, the BS cells must possess intricate mechanisms for sensing any biotic factors that might appear in the vascular tissue, including PAMPS.…”

Section: Introductionmentioning

confidence: 65%

“…To further explore this matter, we evaluated the effect of chitin application on the K leaf of the WT, lyk5 mutants and BS-specific complemented plants (SCR::LYK5/lyk5) in which chitin sensing exists solely in the BS cells. As the BS cells act as a barrier to small solutes 37 , the detached-leaf approach allowed us to feed the chitin directly to the xylem via the petiole, enabling direct contact between the BS cells and the applied chitin 38–40 . In order to ensure the reliability of the chitin treatment, we used two different methods of treatment, a submerged-leaf method and a petiole-feeding method, and used qPCR to examine the quantitative expression of the chitin-induced marker genes AtWRKY29 and AtWRKY30 31 in the WT.…”

Section: Resultsmentioning

confidence: 99%

“…Both AtCERK1 and AtLYK5 RNA are highly expressed in both mesophyll cells and BS cells 38 . Accordingly, our data show that both isolated BS cells and mesophyll cells sense chitin independently, leading to a sharp decrease in Pf.…”

Section: Discussionmentioning

confidence: 99%

“…BS cells were reported to sense abiotic stress signals (e.g., ABA) through the xylem sap and respond to those signals by changing the osmotic water permeability ( P f ) of their membranes. This, in turn, regulates leaf radial hydraulic conductance ( K leaf ), thereby regulating the movement of water into the leaf mesophyll cells 37 In addition, a recent microarray analysis showed that, in Arabidopsis, 45% of the genes that are differentially expressed between BS and mesophyll cells are membrane-related and 20% are transport-related 38 . This strengthens the idea that BS cells are a point of control for the radial transport of solutes.…”

Section: Introductionmentioning

confidence: 99%

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Vascular bundle sheath and mesophyll regulation of leaf water balance in response to chitin

Attia

Dalal

Moshelion

2018

Preprint

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Plants can detect pathogen invasion by sensing pathogen-associated molecular patterns (PAMPs). This sensing process leads to the induction of defense responses. Most PAMP mechanisms of action have been described in the guard cells. Here, we describe the effects of chitin, a PAMP found in fungal cell walls, on the cellular osmotic water permeability (P f ) of the leaf vascular bundle-sheath (BS) and mesophyll cells and its subsequent effect on leaf hydraulic conductance (K leaf ).The BS is a parenchymatic tissue that tightly encases the vascular system. BS cells have been shown to control K leaf through changes in their P f , for example, in response to ABA.It was recently reported that, in Arabidopsis, the chitin receptors chitin elicitor receptor kinase 1 (CERK1) and LYSINE MOTIF RECEPTOR KINASE 5 (LYK5) are highly expressed in the BS, as well as the neighboring mesophyll. Therefore, we studied the possible impact of chitin on these cells.Our results revealed that both BS cells and mesophyll cells exhibit a sharp decrease in P f in response to chitin treatment. In addition, xylem-fed chitin decreased K leaf and led to stomatal closure. However, an Atlyk5 mutant showed none of these responses.Complimenting AtLYK5 specifically in the BS cells (using the SCARECROW promoter) and transient expresion in mesophyll cells each resulted in a response to chitin that was similar to that observed in the wild type. These results suggest that BS and mesophyll cells each play a role in the perception of apoplastic chitin and in initiating chitintriggered immunity.Significance Statement: PAMP perception by plant receptors triggers various defense responses important for plant immunity. Here we provide new insights into a topic that has received a great deal of previous attention, revealing that a chitin immune response is present in additional leaf tissues other than the stomata. Chitin perception by the bundle sheath cells enwrapping the whole leaf vascular system decrease its cellular osmotic permeability and leaf hydraulic conductance. This in turn, leads to hydraulic signals 1 1

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Section: Introductionmentioning

confidence: 65%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Vascular bundle sheath and mesophyll regulation of leaf water balance in response to chitin

Attia

Dalal

Moshelion

2018

Preprint

Self Cite

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“…A tissue-specific distribution of elements is apparent from these distribution maps, with most striking allocation of Ca to epidermis and a substantial allocation of Mg, S and Mn to endodermis, which could be due to transport limitations for these mineral elements connected with the existence of the extracellular diffusion barrier, i.e., Casparian strip. In angiosperm leaves, bundle sheath cells play a similar metabolic role (Leegood 2008;Wigoda et al 2017), although they generally lack Casparian strip. As argued in the introduction, the needle endodermis in gymnosperms resembles the root endodermis both in the morphology as well as in function: it is a bottleneck for outward transport of water and mineral nutrients (Liesche et al 2011) and it contributes to the regulation of carbohydrate export from the needles (Liesche and Schulz 2018).…”

Section: Tissue-specific Distribution Of Elements In Needle Cross-secmentioning

confidence: 99%

Tissue-specific element profiles in Scots pine (Pinus sylvestris L.) needles

Pongrac

Baltrėnaitė

Vavpetič

et al. 2018

Trees

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Key message Element profile signatures of needle tissues differentiated four tissues: epidermis (main contributor: calcium), endodermis (main contributors: magnesium, sulphur and manganese), mesophyll (main contributor: potassium), and transfusion parenchyma (main contributor: zinc). Abstract Distribution of elements in cross-sections of Scots pine (Pinus sylvestris L.) needles was investigated using microproton-induced X-ray emission. Tissue-specific distributions of magnesium (Mg), sulphur (S), calcium (Ca), phosphorus (P), potassium (K), chlorine (Cl), manganese (Mn), iron (Fe), zinc (Zn), aluminium (Al) and silicon (Si) were resolved in a quantitative manner. Distribution maps and tissue-specific concentrations revealed the largest concentration of Ca in epidermis, of Mg, S and Mn in endodermis, of K in mesophyll and phloem and of Zn in transfusion parenchyma. Phosphorus, Cl, Fe, Al and Si did not exhibit apparent tissue-specific distribution. Inverse allocation of P and Ca was observed, a likely mechanism to prevent their precipitation. Taking the area of tissues into account, relative element distribution calculations indicated that mesophyll contained the majority of the elements studied, except Ca, which predominated in the epidermis (79% of total Ca concentration) and Mn, which predominated in the endodermis (40% of total Mn concentration). When considering a complete element profile of a particular tissue, four clusters were differentiated, which generally supported single-element observations. The first cluster differentiated mesophyll, xylem, phloem, transfusion tracheids and Strasburger cells with predominance of K, the second cluster differentiated epidermis on the basis of Ca, the third cluster differentiated endodermis with contributions from Mg, S and Mn, and the fourth cluster differentiated transfusion parenchyma with contribution from Zn. Information on tissue-specific-element allocations will complement structural and functional knowledge of needle tissues and advance our understanding of element/nutrient transfers in Scots pine.

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Hydathode immunity protects the Arabidopsis leaf vasculature against colonization by bacterial pathogens

Paauw¹,

Hulten²,

Chatterjee³

et al. 2023

Current Biology

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Differential gene expression and transport functionality in the bundle sheath versus mesophyll – a potential role in leaf mineral homeostasis

Abstract: The transcriptome analysis of leaf bundle sheath cells compared with mesophyll cells, supported by physiological assays, suggests a potential role of the bundle sheath in radial leaf transport.

Cited by 22 publications

References 58 publications

Vascular bundle sheath and mesophyll regulation of leaf water balance in response to chitin

Vascular bundle sheath and mesophyll regulation of leaf water balance in response to chitin

Tissue-specific element profiles in Scots pine (Pinus sylvestris L.) needles

Hydathode immunity protects the Arabidopsis leaf vasculature against colonization by bacterial pathogens

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