Overexpression of a SDD1-Like Gene From Wild Tomato Decreases Stomatal Density and Enhances Dehydration Avoidance in Arabidopsis and Cultivated Tomato

Abstract

Stomata are microscopic valves formed by two guard cells flanking a pore, which are located on the epidermis of most aerial plant organs and are used for water and gas exchange between the plant and the atmosphere. The number, size and distribution of stomata are set during development in response to changing environmental conditions, allowing plants to minimize the impact of a stressful environment. In Arabidopsis, STOMATAL DENSITY AND DISTRIBUTION 1 (AtSDD1) negatively regulates stomatal density and optimizes transpiration and water use efficiency (WUE). Despite this, little is known about the function of AtSDD1 orthologs in crop species and their wild stress-tolerant relatives. In this study, SDD1-like from the stress-tolerant wild tomato Solanum chilense (SchSDD1-like) was identified through its close sequence relationship with SDD1-like from Solanum lycopersicum and AtSDD1. Both Solanum SDD1-like transcripts accumulated in high levels in young leaves, suggesting that they play a role in early leaf development. Arabidopsis sdd1-3 plants transformed with SchSDD1-like under a constitutive promoter showed a significant reduction in stomatal leaf density compared with untransformed sdd1-3 plants. Additionally, a leaf dehydration shock test demonstrated that the reduction in stomatal abundance of transgenic plants was sufficient to slow down dehydration. Overexpression of SchSDD1-like in cultivated tomato plants decreased the stomatal index and density of the cotyledons and leaves, and resulted in higher dehydration avoidance. Taken together, these results indicate that SchSDD1-like functions in a similar manner to AtSDD1 and suggest that Arabidopsis and tomatoes share this component of the stomatal development pathway that impinges on water status.

The Role of Proteases in Determining Stomatal Development and Tuning Pore Aperture: A Review

“…Transcripts were detected in meristemoids (stomatal initials) and GMCs, but were absent in mature stomata indicating a developmental rather than a constitutive role of SSD1 in stomatal formation [35]. In agreement to these results, Morales-Navarro et al [36] reported increased transcription of the gene in growing tomato leaves suggesting the involvement of SDD1 in their development. SDD1 is a negative regulator of stomatal development, since it lessens both the formation of stomatal complexes and the number of stomata produced per stomatal complex [34].…”

“…This contact between neighboring stomata has been related to pitfalls, including reduced carbon assimilation and impaired stomatal responses to external cues [22]. Moreover, similar functionality of SDD1 has been reported in Arabidopsis and tomato by Morales-Navarro et al [36]. Although SDD1 strongly influences stomatal development, the proteolysis of EPF members by the SDD1 remains elusive [31,39].…”

“…A decrease in stomatal density, as a result of SDD1 overexpression, has been generally correlated to enhanced water use efficiency and drought tolerance [37,38]. Moreover, SDD1 regulates the orientation of spacing divisions in neighboring cells [36]. In sdd1-1 mutants, the principle of maintaining one epidermal cell spacing between adjacent stomata was violated, as a result of misoriented spacing divisions, thus forming stomatal clusters (i.e., two or more stomata touching) [34].…”

YODA Kinase Controls a Novel Immune Pathway of Tomato Conferring Enhanced Disease Resistance to the Bacterium Pseudomonas syringae

“…Stomatal and pavement cell densities and stomatal indexes were scored in the terminal leaflet of the third leaf of 25-day-old plants. Leaflets were hand-excised, fixed, and clarified as indicated in Morales-Navarro et al (2018) with minor modifications. Plant material was fixed in ethanol:acetic acid 9:1 (v/v) for 48 h, rehydrated through ethanol series, and cleared in a chloral hydrate:glycerol:water solution (8:1:2, w/v/v) for 48 h. The abaxial epidermis was inspected with differential interference contrast (DIC) under a Nikon Eclipse 90i upright microscope and a DXM1200C camera for image acquisition.…”

Crop Biotechnology for Improving Drought Tolerance: Targets, Approaches, and Outcomes

“…Although SDD1's mechanism of action is currently unclear (Pillitteri and Dong, 2013), its overexpression reduces stomatal density. Overexpression of ZmSDD1 has been exploited to improve drought resistance in maize (Liu et al, 2015) and recently a wild tomato SDD1-like gene SchSDD1 was shown to improve water deficit tolerance in cultivated tomato (Morales-Navarro et al, 2018). However, it remains unclear how SDD1 overexpression affects seed and fruit development as no harvest or yield data were reported for these species in either studies.…”