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Agave angustifolia albino plantlets lose stomatal physiology function by changing the development of the stomatal complex due to a molecular disruption

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Abstract

Stomatal development is regulated by signaling pathways that function in multiple cellular programs, including cell fate and cell division. However, recent studies suggest that molecular signals are affected by CO2 concentration, light intensity, and water pressure deficit, thereby modifying distribution patterns and stomatic density and likely other foliar features as well. Here, we show that in addition to lacking chloroplasts, the albino somaclonal variants of Agave angustifolia Haw present an irregular epidermal development and morphological abnormalities of the stomatal complex, affecting the link between the stomatal conductance, transpiration and photosynthesis, as well as the development of the stoma in the upper part of the leaves. In addition, we show that changes in the transcriptional levels of SPEECHLESS (SPCH), TOO MANY MOUTHS (TMM), MITOGEN-ACTIVATED PROTEIN KINASE 4 and 6 (MAPK4 and MAPK6) and FOUR LIPS (FLP), all from the meristematic tissue and leaf, differentially modulate the stomatal function between the green, variegated and albino in vitro plantlets of A. angustifolia. Likewise, we highlight the conservation of microRNAs miR166 and miR824 as part of the regulation of AGAMOUS-LIKE16 (AGL16), recently associated with the control of cell divisions that regulate the development of the stomatal complex. We propose that molecular alterations happening in albino cells formed from the meristematic base can lead to different anomalies during the transition and specification of the stomatal cell state in leaf development of albino plantlets. We conclude that the molecular alterations in the meristematic cells in albino plants might be the main variable associated with stoma distribution in this phenotype.

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Funding

This work was funded by CONSEJO NACIONAL DE CIENCIA Y TECNOLOGÍA to CD-L-P (CB2016-285898 and CB2016-286368) and CONACYT-scholarships to SHC (271240).

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Authors and Affiliations

  1. Centro de Investigación Científica de Yucatán A.C., Unidad de Biotecnología, Calle 43 N°130 x 32 y 34, Chuburná de Hidalgo, 97205, Mérida, Yucatán, Mexico

    Hernández-Castellano Sara, Us-Camas Rosa & De-la-Peña Clelia

  2. Centro de Investigación Científica de Yucatán A.C., Unidad de Bioquímica y Biología Molecular de Plantas, Calle 43 N° 130 x 32 y 34, Chuburná de Hidalgo, 97205, Mérida, Yucatán, Mexico

    Kú-Gonzalez Angela

  3. CONACYT-Instituto Tecnológico de Conkal, Avenida Tecnológico s/n Conkal, 97345, Mérida, Yucatán, Mexico

    Garruña-Hernández René

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  1. Hernández-Castellano Sara
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  2. Garruña-Hernández René
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  3. Us-Camas Rosa
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  4. Kú-Gonzalez Angela
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  5. De-la-Peña Clelia
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Contributions

SHC conducted most of the experiments, conceived and designed the experiments, and drafted the article. RGH helped in data collection and parameter physiological sample preparation. RUS helped in design primer and sample preparation. AKG helped in data collection and microscopy sample preparation. CD-L-P and SHC coordinated the project, conceived and designed the experiments and edited the manuscript.

Corresponding author

Correspondence to De-la-Peña Clelia.

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Communicated by Akhilesh K. Tyagi.

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Significance statement: Agave albino plantlets have a stomatal pattern and a stomatal density not seen elsewhere in plants. Further, the albino leaf does not respond photosynthetically, suggesting that it does not have photosynthetically active mesophyll cells. However, our data show that despite the dramatic changes in physiology in the albino region of the variegated plant, the overall responsiveness of guard cells to CO2 remains unaltered. Although much physiological data are available about how stomata functionality changes in response to environmental conditions (light, CO2, and humidity), the molecular and epigenetic mechanisms that regulate this process are poorly understood. In this work, we have shown that the molecular alteration in the new cell in the leaves compared to the meristematic tissue might be the main variable associated with stoma distribution in albino plants. This finding hints at the importance of stomatal origins and functions.

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Supplementary Figure 1

. Patterns of stomatal distribution and autofluorescence emission of chlorophyll in guard cells of the stomatal complex between leaf tissue in green (G), green region (GV), and albino region (AV) of the variegated (V) and albino (A) leaves. (JPEG 2993 kb)

Supplementary Figure 2

. Analysis of the stomatal complex from the measurements made in the images obtained by confocal laser microscopy in the abaxial and adaxial epidermis in the basal, middle and apical regions of green leaves (G), green region (GV) and albino region (AV) of the variegated (V) and albino (A) leaves. (JPEG 2529 kb)

Supplementary Figure 3

. RT-qPCR efficiency of the miR166, miR824 and SnU6 gene reference Ct: cycle threshold value (mean ± SD; n = 3); E: qPCR efficiencies, E = 10[–1/slope]. (JPEG 2407 kb)

Supplementary Figure 4

. Density and index stomatal on the adaxial and abaxial side of the seedling leaf of A. angustifolia Haw plantlets G, V and A, grown under culture conditions in vitro. The letters indicate the significant differences between phenotypes by region analyzed (Tukey, α = 0.05), n = 8. Ap, apical; Mi, medium; B, basal (JPEG 2526 kb)

Supplementary material 5 (DOCX 23 kb)

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Sara, HC., René, GH., Rosa, UC. et al. Agave angustifolia albino plantlets lose stomatal physiology function by changing the development of the stomatal complex due to a molecular disruption. Mol Genet Genomics 295, 787–805 (2020). https://doi.org/10.1007/s00438-019-01643-y

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