Abstract Grafting has been adopted for a wide range of crops to enhance productivity and resilience; for example, grafting of Solanaceous crops couples disease-resistant rootstocks with scions that produce high-quality fruit. However, incompatibility severely limits the application of grafting and graft incompatibility remains poorly understood. In grafts, immediate incompatibility results in rapid death, but delayed incompatibility can take months or even years to manifest, creating a significant economic burden for perennial crop production. To gain insight into the genetic mechanisms underlying this phenomenon, we developed a model system using heterografting of tomato (Solanum lycopersicum) and pepper (Capsicum annuum). These grafted plants express signs of anatomical junction failure within the first week of grafting. By generating a detailed timeline for junction formation, we were able to pinpoint the cellular basis for this delayed incompatibility. Furthermore, we inferred gene regulatory networks for compatible self-grafts and incompatible heterografts based on these key anatomical events, which predict core regulators for grafting. Finally, we examined the role of vascular development in graft formation and uncovered SlWOX4 as a potential regulator of graft compatibility. Following this predicted regulator up with functional analysis, we show that Slwox4 homografts fail to form xylem bridges across the junction, demonstrating that indeed, SlWOX4 is essential for vascular reconnection during grafting, and may function as an early indicator of graft failure.
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Anatomical and biophysical basis for graft incompatibility within the Solanaceae
Interspecies grafting is an economically relevant technique that allows beneficial shoot and root combinations from separate species to be combined. One hypothesis for the basis of graft compatibility revolves around taxonomic relatedness. To test how phylogenetic distance affects interspecific graft compatibility within the economically important Solanaceae subfamily, Solanoideae, we characterized the anatomical and biophysical integrity of graft junctions between four species: tomato (Solanum lycopersicum), eggplant (Solanum melongena), pepper (Capsicum annuum), and groundcherry (Physalis pubescens). We analyzed the survival, growth, integrity, and cellular composition of the graft junctions. Utilizing various techniques, we were able to quantitatively assess compatibility among the interspecific grafts. Even though most of our graft combinations could survive, we show that only intrageneric combinations between tomato and eggplant are compatible. Unlike incompatible grafts, the formation of substantial vascular reconnections between tomato and eggplant in the intrageneric heterografts likely contributed to biophysically stable grafts. Furthermore, we identified 10 graft combinations that show delayed incompatibility, providing a useful system to pursue deeper work into graft compatibility. This work provides new evidence that graft compatibility may be limited to intrageneric combinations within the Solanoideae subfamily. Further research amongst additional Solanaceous species can be used to test the extent to which our hypothesis applies to this family.
more » « less- NSF-PAR ID:
- 10421289
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- ISSN:
- 0022-0957
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Plants have mechanisms to recognize and reject pollen from other species. Although widespread, these mechanisms are less well understood than the self‐incompatibility (
SI ) mechanisms plants use to reject pollen from close relatives. Previous studies have shown that some interspecific reproductive barriers (IRB s) are related toSI in the Solanaceae. For example, the pistilSI proteins S‐RN ase andHT protein function in a pistil‐sideIRB that causes rejection of pollen from self‐compatible (SC ) red/orange‐fruited species in the tomato clade. However, S‐RN ase‐independentIRB s also clearly contribute to rejecting pollen from these species. We investigated S‐RN ase‐independent rejection ofSolanum lycopersicum pollen bySC Solanum pennellii LA 0716,SC .Solanum habrochaites LA 0407, andSC Solanum arcanum LA 2157, which lack functional S‐RN ase expression. We found that all three accessions expressHT proteins, which previously had been known to function only in conjunction with S‐RN ase, and then usedRNA i to test whether they also function in S‐RN ase‐independent pollen rejection. SuppressingHT SC S. pennellii LA 0716 allowsS. lycopersicum pollen tubes to penetrate farther into the pistil inHT HT SC .Solanum habrochaites LA 0407 and inSC S. arcanum LA 2157 allowsS. lycopersicum pollen tubes to penetrate to the ovary and produce hybrids that, otherwise, would be difficult to obtain. Thus,HT proteins are implicated in both S‐RN ase‐dependent and S‐RN ase‐independent pollen rejection. The results support the view that overall compatibility results from multiple pollen–pistil interactions with additive effects. -
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Societal Impact Statement Fleshy fruits provide humans with many flavorful and nutritious crops. Understanding the diversity of these plants is fundamental to managing agriculture and food security in a changing world. This study surveyed fruit trait variation across species of tomato wild relatives and explored associations among color, size, shape, sugars, and acids. These wild tomato species native to South America can be interbred with the economically important cultivated tomato. Beyond its application to tomatoes, deepening our knowledge of how fruit traits evolve together is valuable to crop improvement efforts aimed at breeding more nutritious and appealing varieties of fruits.
Summary Fleshy fruits display a striking diversity of traits, many of which are important for agriculture. The evolutionary drivers of this variation are not well understood, and most studies have relied on variation found in the wild. Few studies have explored this question on a fine‐grained scale with a group of recently diverged species while controlling for environmental effects.
We developed the tomato clade as a novel system for fruit trait evolution research by presenting the first common garden‐based systematic survey of variation and phylogenetic signal in color, nutrition, and morphology traits across all 13 species of tomato wild relatives (
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Abstract The nuclear lamina in plant cells is composed of plant-specific proteins, including nuclear matrix constituent proteins (NMCPs), which have been postulated to be functional analogs of lamin proteins that provide structural integrity to the organelle and help stabilize the three-dimensional organization of the genome. Using genomic editing, we generated alleles for the three genes encoding NMCPs in cultivated tomato (Solanum lycopersicum) to determine if the consequences of perturbing the nuclear lamina in this crop species were similar to or distinct from those observed in the model Arabidopsis thaliana. Loss of the sole NMCP2-class protein was lethal in tomato but is tolerated in Arabidopsis. Moreover, depletion of NMCP1-type nuclear lamina proteins leads to distinct developmental phenotypes in tomato, including leaf morphology defects and reduced root growth rate (in nmcp1b mutants), compared with cognate mutants in Arabidopsis. These findings suggest that the nuclear lamina interfaces with different developmental and signaling pathways in tomato compared with Arabidopsis. At the subcellular level, however, tomato nmcp mutants resembled their Arabidopsis counterparts in displaying smaller and more spherical nuclei in differentiated cells. This result argues that the plant nuclear lamina facilitates nuclear shape distortion in response to forces exerted on the organelle within the cell.
