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Riddled with holes: Understanding air space formation in plant leaves

['Christopher D. Whitewoods', 'Sainsbury Laboratory', 'University Of Cambridge', 'Cambridge', 'United Kingdom']

Date: 2021-12

Within a leaf, air spaces are spatially patterned. Aquatic plant leaves often look like waggon wheels in cross section, with enlarged air spaces arranged radially with each separated by a single file of cells (Fig 1A). In terrestrial leaves, air spaces are patterned along the adaxial/abaxial axis, with small spaces between the adaxial palisade mesophyll cells and large spaces between the abaxial spongy mesophyll cells, with particularly large cavities adjacent to stomata.

Adaxial and abaxial patterning in air space development.

The adaxial/abaxial patterning of mesophyll cell types is controlled by well-known genetic regulators of adaxial/abaxial leaf patterning, including genes from the HDZIPIII (adaxial) and KANADI (abaxial) families (reviewed in [21]). For example, A. thaliana or Antirrhinum majus plants lacking adaxial identity form leaves containing only spongy mesophyll cells [22,23]. However, although containing only spongy mesophyll cells, abaxialised leaves contain few, small air spaces [22,23]. This suggests that large air spaces are not simply a product of spongy mesophyll identity. Abaxialised leaves also fail to form a leaf blade and are instead needle shaped, suggesting that expansion of the leaf blade is necessary for air spaces to form in flat leaves and that air spaces may be an emergent property of multicellular leaf growth rather than an intrinsic part of spongy mesophyll cell identity.

These observations suggest that plants localise air space formation to certain regions of the leaf and within certain cell types. However, beyond adaxial and abaxial identity genes, factors that control air space size and arrangement are relatively unknown. This is partly down to difficulties visualising internal tissues and screening for mutants. Indeed, no genes are known to regulate palisade versus spongy mesophyll cell identity and associated air space formation.

Thus far, 2 factors are known to regulate leaf air space patterning: stomatal and chloroplast signalling.

Stomatal signalling in air space development. The observation that large air spaces are positioned adjacent to stomata in many species [9,24] (Fig 3) suggests that stomata themselves may regulate the position of large spaces. This has been confirmed by recent work showing that stomatal density and air space volume are positively correlated with both A. thaliana and wheat [24,25]. Experiments suggest that substomatal air spaces form only adjacent to mature, open stomata [24,25]. For example, in the A. thaliana focl1-1 mutant, stomatal pores are partially occluded by a layer of cuticle, resulting in reduced gas exchange [24]. In these plants, the correlation between stomatal density and air space volume is partially broken, suggesting that the physiological function of stomata may signal to promote mesophyll air space formation. These data do not rule out a molecular signal from mature guard cells to promote air space formation, but they do suggest that air space formation is promoted by the functioning of the open pore itself, likely via gas exchange. The nature of the gaseous signal is still unclear, but the 2 most likely candidates are CO 2 or H 2 O (water vapour). Future work experimentally altering gas concentrations may be able to identify the gas involved and promises to uncover how the physiological demands of the plant influence development to optimise leaf structure and balance water use efficiency and photosynthesis.

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TIFF original image Download: Fig 3. Environmental and physiological signals control air space formation. Gas exchange via stomata promotes air space formation around stomata (blue arrow), chloroplast signalling reduces air space formation throughout the mesophyll and promotes palisade mesophyll identity (red arrows), and light intensity and temperature regulate air space formation, but their effects remain poorly characterised (yellow arrows). https://doi.org/10.1371/journal.pbio.3001475.g003

There may also be a role for molecular signals beyond gas exchange, as mutations in the receptor genes ERECTA (ER) or TOO MANY MOUTHS (TMM) alter stomatal density and break the observed correlation between stomatal density and air space patterning. This suggests they may provide a molecular link between stomatal and mesophyll development [25,26]. Intriguingly, the mesophyll-expressed STOMAGEN protein is known to move to the epidermis and bind ER and TMM to alter stomatal density [27,28]. This suggests that there may be a feedback loop between the mesophyll and epidermis that fine-tunes stomatal density and air space patterning. However, the interplay between these factors and gas exchange is poorly understood.

Chloroplast signalling in air space development. The role of chloroplasts in air space development was demonstrated by analysis of reticulate mutants in A. thaliana. This class of mutants have pale green leaves with dark green veins. In most reticulate mutants, the pale lamina is caused by a reduction in mesophyll cell density and corresponding increase in air space volume within the leaf (e.g., [29,30]). Most described reticulate mutants are affected in genes that control chloroplast biogenesis or metabolism, resulting in plants with chloroplasts of reduced number and function. These include mutations in the genes scabra3 [31], differential development of vascular associated cells 1 (dov1) [32], cab underexpressed1 (cue1) [33], and venosa (ven) 3 and 6 [34] (reviewed in [35]). Other reticulate mutations, such as in the reticulata-related gene family [29], have no effect on chloroplast development, but the affected genes encode proteins that localise to chloroplasts, further supporting a link between chloroplasts and air space formation.

The observation that leaves with compromised chloroplasts have larger air spaces suggests that chloroplasts signal to mesophyll cells to regulate mesophyll cell proliferation and air space volume. This is supported by data from A. thaliana and A. majus leaves in which chloroplast development is blocked genetically or with spectinomycin (an inhibitor of plastid protein synthesis). Leaves of these plants contain sectors of cells lacking fully developed chloroplasts. In these chloroplast-deficient sectors, palisade mesophyll cells are absent, producing a pale leaf with large air spaces composed largely of spongy mesophyll cells [36,37]. These data suggest a role for chloroplast signalling in both cell identity and air space formation in the mesophyll. However, whether functional chloroplasts signal to enhance mesophyll cell proliferation and reduce air space formation or defective chloroplasts signal to reduce mesophyll cell proliferation and increase air spaces remain unclear [38].

As the above loss of palisade cells is restricted to chloroplast deficient sectors, it is likely that signalling from the chloroplast to regulate palisade identity and air space formation is, at least in part, cell autonomous (Fig 3). However, several of the genes mutated in reticulate mutants are expressed preferentially or exclusively in bundle sheath cells surrounding the vasculature, adding a spatial element to chloroplast regulation of air space patterning [29,39] (reviewed in [35]; Fig 3). This has led to the suggestion that plastids in the bundle sheath may either transmit a molecular signal to regulate mesophyll growth [40,41] or supply necessary metabolites for mesophyll cell growth and division [32]. Any molecular signal is unknown, but the phenylpropanoid-derived secondary metabolite dehydrodiconiferyl alcohol glucoside (DCG) is known to promote cell division and expansion in tobacco [42,43] and is reduced in the reticulate mutant cue1, making it a possible candidate [41]. However, its production in and movement from the bundle sheath have not been demonstrated. Other candidates for a possible molecular signal include reactive oxygen species, small interfering RNAs (siRNAs), hormones, other metabolites, or proteins, all of which are known to be mobile and regulate developmental processes. Evidence that the bundle sheath supplies metabolites to the mesophyll is supported by data showing that several reticulate mutants (including cue1 [41,44] and ven3 and 6 [34]) are deficient in amino acids and nucleotides, and exogenous application of these metabolites often rescues the phenotype. Further investigation is needed to understand exactly how chloroplasts signal to mesophyll cells to regulate cell identity and growth, but emerging evidence suggests that plastid localised proteins, such as ENLARGED FIL EXPRESSING DOMAIN 2 (ENF2) interact with adaxial/abaxial patterning factors to position spongy versus palisade mesophyll cell identity along the adaxial/abaxial axis, providing a tantalising link to well-known regulators of leaf development [45].

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001475

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