Genetic Architecture and Molecular Networks Underlying Leaf Thickness in Desert-Adapted TomatoSolanum pennellii

Abstract

Thicker leaves allow plants to grow in water-limited conditions. However, our understanding of the genetic underpinnings of this highly functional leaf shape trait is poor. We used a custom-built confocal profilometer to directly measure leaf thickness in a set of introgression lines (ILs) derived from the desert tomato species Solanum pennellii, and identified quantitative trait loci (QTL). We report evidence of a complex genetic architecture of this trait and roles for both genetic and environmental factors. Several ILs with thick leaves have dramatically elongated palisade mesophyll cells and, in some cases, increased leaf ploidy. We characterized thick ILs 2-5 and 4-3 in detail and found increased mesophyll cell size and leaf ploidy levels, suggesting that endoreduplication underpins leaf thickness in tomato. Next, we queried the transcriptomes and inferred Dynamic Bayesian Networks of gene expression across early leaf ontogeny in these lines to compare the molecular networks that pattern leaf thickness. We show that thick ILs share S. pennellii-like expression profiles for putative regulators of cell shape and meristem determinacy, as well as a general signature of cell cycle related gene expression. However, our network data suggest that leaf thickness in these two lines is patterned by at least partially distinct mechanisms. Consistent with this hypothesis, double homozygote lines combining introgression segments from these two ILs show additive phenotypes including thick leaves, higher ploidy levels and larger palisade mesophyll cells. Collectively, these data establish a framework of genetic, anatomical, and molecular mechanisms that pattern leaf thickness in desert-adapted tomato.

Multiple steps of leaf thickening during sun‐leaf formation in Arabidopsis

“…Cell enlargement often occurs concomitantly with increases in ploidy levels during organogenesis in some plant species (Traas et al ., ; Kondorosi et al ., ; Sugimoto‐Shirasu and Roberts, ). Regarding leaf‐thickness growth, corresponding increases in cell size and ploidy levels were reported in Solanaceae species (Gauhl, ; Coneva et al ., ). In a recent study, the light‐shift experiment in Arabidopsis showed that exposure to HL conditions promoted the endocycle in Arabidopsis (Mohammed et al ., ).…”

Modern phenotyping platforms and their application in plant biology and agriculture

“…Система была успешно использована для целого ряда фундаментальных и прикладных исследований. Например, детально изучена динамика фенотипических ответов С 4 -растений на дефицит азота и засуху [32]; найдена группа генов, контролирующих геометрию листа пасленовых [33]; описана эффективность функционирования фотосистемы II арабидопсиса и кукурузы [34] и др.…”

Trait discovery and editing in tomato

“…Using two well known QTL/gene, fw2.2 and beta‐carotene ( B ), they demonstrated the high‐resolution mapping offered by the population. The genome of the S. pennellii accession was sequenced (Bolger et al ., ) and BILs enabled the characterization of QTL involved in yield (Soyk et al ., ), leaf shape (Fulop et al ., ), leaf thickness (Coneva et al ., ), and day length response (Müller et al ., ; Soyk et al ., ).…”

“…For nearly two decades, ’omics technologies including transcriptomics, proteomics, and metabolomics have been used alone or in combination to discover genes and networks underlying various traits of interest in tomato. Examples of these are rootstock grafting (Ntatsi et al ., ), effect of root mycorhization on fruit quality (Zouari et al ., ), meristem maturation and inflorescence architecture (Park et al ., ; Soyk et al ., ), leaf morphology and thickness (Koenig et al ., ; Coneva et al ., ), glandular trichome metabolism (Balcke et al ., ), seed composition (Toubiana et al ., ), fruit set and parthenocarpy (Wang et al ., ; Ruiu et al ., ), and fruit development, ripening, and composition (Carrari et al ., ; Faurobert et al ., ; Mintz‐Oron et al ., ; Mounet et al ., ; Matas et al ., ; Osorio et al ., ; Itkin et al ., ; Pan et al ., ; Pattison et al ., ; Fernandez‐Moreno et al ., ; Szymanski et al ., ; Li et al ., ; Shinozaki et al ., ; Stevens et al ., ). While fruit studies outnumber all others, considerable efforts have also been devoted to the study of abiotic stress, including heat (Keller and Simm, ), cold (Cruz‐Mendívil et al ., ; Barrero‐Gil et al ., ; Ntatsi et al ., ), water limitation (Albert et al ., ), salinity stress (Zhang et al ., ) and nutrient deficiency (Zamboni et al ., ), and of plant reaction to biotic stress, causes of which include viruses (Ramesh et al ., ), bacteria (French et al ., ), fungi (Blanco‐Ulate et al ., ; Ghosh et al ., ), and nematodes (Święcicka et al ., ).…”