Bundle sheath cells and cell-specific plastid development in <i>Arabidopsis</i> leaves

Kinsman, Elizabeth A.; Pyke, Kevin

doi:10.1242/dev.125.10.1815

Cited by 148 publications

(22 citation statements)

References 30 publications

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“…The development of Arabidopsis first leaves has been described previously in detail (Amalraj et al., 2020; Candela, Martinez‐Laborda, & Micol, 1999; Donnelly, Bonetta, Tsukaya, Dengler, & Dengler, 1999; Kang & Dengler, 2002; Kang & Dengler, 2004; Kinsman & Pyke, 1998; Larkin, Young, Prigge, & Marks, 1996; Mattsson et al., 1999; Mattsson, Ckurshumova, & Berleth, 2003; Pyke, Marrison, & Leech, 1991; Telfer & Poethig, 1994). Briefly, at 1 DAG the first leaf is recognizable as a semi‐spherical primordium (Fig.…”

Section: Commentarymentioning

confidence: 99%

Confocal Imaging of Developing Leaves

Linh

Scarpella

2022

Current Protocols

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Questions in developmental biology are most frequently addressed by using fluorescent markers of otherwise invisible cell states. In plants, such questions can be addressed most conveniently in leaves. Indeed, from the formation of stomata and trichomes within the leaf epidermis to that of vein networks deep into the leaf inner tissue, leaf cells and tissues differentiate anew during the development of each leaf. Moreover, leaves are produced in abundance and are easily accessible to visualization and perturbation. Yet a detailed procedure for the perturbation, dissection, mounting, and imaging of developing leaves has not been described. Here we address this limitation (1) by providing robust, step‐by‐step protocols for the local application of the plant hormone auxin to developing leaves and for the routine dissection and mounting of leaves and leaf primordia, and (2) by offering practical guidelines for the optimization of imaging parameters for confocal microscopy. We describe the procedure for the first leaves of Arabidopsis, but the same approach can be easily applied to other leaves of Arabidopsis or to leaves of other plants. © 2022 Wiley Periodicals LLC. Support Protocol 1: Preparation of plant growth medium Support Protocol 2: Preparation of growth medium plates Basic Protocol 1: Seed sterilization, sowing, and germination, and seedling growth Support Protocol 3: Preparation of IAA–lanolin paste Basic Protocol 2: Application of IAA–lanolin paste to 3.5‐DAG first leaves Basic Protocol 3: Dissection of 3‐ to 6‐DAG first leaves and leaf primordia Basic Protocol 4: Dissection of 1‐ and 2‐DAG first‐leaf primordia Basic Protocol 5: Mounting of dissected leaves and leaf primordia Support Protocol 4: Quality check of mounted leaves and leaf primordia by fluorescence microscopy Basic Protocol 6: Imaging of mounted leaves and leaf primordia by confocal microscopy

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Section: Commentarymentioning

confidence: 99%

Confocal Imaging of Developing Leaves

Linh

Scarpella

2022

Current Protocols

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“…The development of Arabidopsis leaves has been described previously [ 30 , 32 – 34 , 46 – 51 ]. Briefly, at 2 DAG the first leaf is recognizable as a cylindrical primordium with a midvein at its center ( Fig 2A ).…”

Section: Resultsmentioning

confidence: 99%

“…(ii) lateral veins that branch from the midvein and join distal veins to form closed loops; (iii) minor veins that branch from midvein and loops and either end freely or join other veins; and (iv) minor veins and loops that curve near the leaf margin and give the vein network a scalloped outline [5,[30][31][32][33][34][35][36][37][38] (Fig 1A , 1B and 1F). Within individual veins, vascular elements are connected end to end and are aligned along the length of the vein, and free vein ends are as narrow as the rest of the vein (Fig 1G).…”

Section: Control Of Vein Patterning By Regulated Pd Aperturementioning

confidence: 99%

“…The development of Arabidopsis leaves has been described previously [30,[32][33][34][46][47][48][49][50][51]. Briefly, at 2 DAG the first leaf is recognizable as a cylindrical primordium with a midvein at its center (Fig 2A In 2.5-DAG primordia of E2331>>erGFP/YFP, in which GAL4 expression is activated at early stages of vein development [52], YFP was detected throughout the 2.5-DAG primordium, even though erGFP was only expressed in the midvein ( (A-E) Veins form sequentially during Arabidopsis leaf development: The formation of the midvein is followed by the formation of the first loops of veins ("first loops"); the formation of first loops is followed by that of second loops and minor veins; and the formation of second loops and minor veins is followed by that of third loops.…”

Section: Pd Permeability Changes During Leaf Developmentmentioning

confidence: 99%

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Leaf vein patterning is regulated by the aperture of plasmodesmata intercellular channels

Linh

Scarpella

2022

PLoS Biol

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To form tissue networks, animal cells migrate and interact through proteins protruding from their plasma membranes. Plant cells can do neither, yet plants form vein networks. How plants do so is unclear, but veins are thought to form by the coordinated action of the polar transport and signal transduction of the plant hormone auxin. However, plants inhibited in both pathways still form veins. Patterning of vascular cells into veins is instead prevented in mutants lacking the function of the GNOM (GN) regulator of auxin transport and signaling, suggesting the existence of at least one more GN-dependent vein-patterning pathway. Here we show that in Arabidopsis such a pathway depends on the movement of auxin or an auxin-dependent signal through plasmodesmata (PDs) intercellular channels. PD permeability is high where veins are forming, lowers between veins and nonvascular tissues, but remains high between vein cells. Impaired ability to regulate PD aperture leads to defects in auxin transport and signaling, ultimately leading to vein patterning defects that are enhanced by inhibition of auxin transport or signaling. GN controls PD aperture regulation, and simultaneous inhibition of auxin signaling, auxin transport, and regulated PD aperture phenocopies null gn mutants. Therefore, veins are patterned by the coordinated action of three GN-dependent pathways: auxin signaling, polar auxin transport, and movement of auxin or an auxin-dependent signal through PDs. Such a mechanism of tissue network formation is unprecedented in multicellular organisms.

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“…Several maize genes are known for their role in chloroplast development specifically in BS cells (Kinsman and Pyke, 1998), such as GOLDEN2 and related transcription factors (Hall et al, 1998;Rossini et al, 2001), and BUNDLE SHEATH DEFECTIVE 2 (BSD2), which encodes a DnaJ-like protein that regulates rbcL expression in the BS cells (Brutnell et al, 1999). When a GOLDEN2-like gene from rice or the BSD2 gene from maize was overexpressed in rice or maize, chloroplast development was induced in the BS, indicating that these two genes are master regulators of chloroplast development (Wang et al, 2017).…”

Section: Chloroplast Size and Numbermentioning

confidence: 99%

Challenges and Approaches to Crop Improvement Through C3-to-C4 Engineering

Cui

2021

Front. Plant Sci.

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With a rapidly growing world population and dwindling natural resources, we are now facing the enormous challenge of increasing crop yields while simultaneously improving the efficiency of resource utilization. Introduction of C4 photosynthesis into C3 crops is widely accepted as a key strategy to meet this challenge because C4 plants are more efficient than C3 plants in photosynthesis and resource usage, particularly in hot climates, where the potential for productivity is high. Lending support to the feasibility of this C3-to-C4 engineering, evidence indicates that C4 photosynthesis has evolved from C3 photosynthesis in multiple lineages. Nevertheless, C3-to-C4 engineering is not an easy task, as several features essential to C4 photosynthesis must be introduced into C3 plants. One such feature is the spatial separation of the two phases of photosynthesis (CO2 fixation and carbohydrate synthesis) into the mesophyll and bundle sheath cells, respectively. Another feature is the Kranz anatomy, characterized by a close association between the mesophyll and bundle sheath (BS) cells (1:1 ratio). These anatomical features, along with a C4-specific carbon fixation enzyme (PEPC), form a CO2-concentration mechanism that ensures a high photosynthetic efficiency. Much effort has been taken in the past to introduce the C4 mechanism into C3 plants, but none of these attempts has met with success, which is in my opinion due to a lack of system-level understanding and manipulation of the C3 and C4 pathways. As a prerequisite for the C3-to-C4 engineering, I propose that not only the mechanisms that control the Kranz anatomy and cell-type-specific expression in C3 and C4 plants must be elucidated, but also a good understanding of the gene regulatory network underlying C3 and C4 photosynthesis must be achieved. In this review, I first describe the past and current efforts to increase photosynthetic efficiency in C3 plants and their limitations; I then discuss a systems approach to tackling down this challenge, some practical issues, and recent technical innovations that would help us to solve these problems.

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Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves

Cited by 148 publications

References 30 publications

Confocal Imaging of Developing Leaves

Confocal Imaging of Developing Leaves

Leaf vein patterning is regulated by the aperture of plasmodesmata intercellular channels

Challenges and Approaches to Crop Improvement Through C3-to-C4 Engineering

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