The invisible light stimulus: Physiological mechanisms of yield improvement by far-red radiation in tomato

Tomato (Solanum lycopersicum) is not only one of the world’s most important horticultural crops but also one of the main crops for greenhouse production. Modern greenhouse production is not only expected to increase yield and product quality but also to achieve that sustainably. The horticultural sector has long been at the front of technological advances in crop production. Light is one of the most important environmental factors in crop production, and it is a common practice to apply supplementary lighting in greenhouses at locations where low daily light integral is low during the growing season to ensure a year-round production. In these greenhouses, the high-pressure sodium (HPS) lamps are the most used light source due to their low price and decent efficacy in converting electric power to light photons. Despite their popularity, HPS lamps also have disadvantages such as excessive heat emission and inflexibility in the light spectrum. Recently, light-emitting-diodes (LEDs) emerge as an exciting alternative to HPS lamps. LED lighting has over 60% higher efficacy, low heat emission, and can be customized to provide different intensities and spectra. The popularity of LED lighting in horticultural production also stimulated research on the spectral effects of supplementary lighting on plant growth and development, even extending the research to the spectrum that is beyond photosynthetically active radiation (400-700 nm). Far-red radiation (FR), which has a wavelength between 700-800 nm, has been extensively studied due to its role in plant’s neighbor detection and sensing of shading. Interestingly, several studies point towards yield increases as a result of additional FR in several crops. This thesis aims to understand the effect of adding FR on the responses of growth and development of both young and fruit-bearing tomato plants. Specifically, 1) to evaluate and explain genotypic variation in dry mass production of young tomato plants in response to FR, 2) to quantify the FR effect on dry mass partitioning between shoot and root in young tomato plants and explain the regulatory mechanisms, 3) to evaluate whether FR leads a trade-off between growth and plant immunity, and 4) to quantify the FR effect on tomato fruit yield and study the physiological and molecular pathways by which FR regulates this response.

Chapter 1 described the status of greenhouse tomato production, and what is known about plants’ responses to FR. The development of supplementary lighting used in greenhouse tomato production was described, and a comparison was made between the more efficient LED lighting and conventional HPS lighting. Here, known effects on the perception of FR and its regulation of shade avoidance responses were summarized. The latest studies were summarized, and they pointed towards a positive effect of FR on tomato yield. However, these studies did not reveal a clear mechanism for this yield improvement. Moreover, there was contradiction and variation between the results, suggesting that species and even different genotypes within the same species may respond differently to FR. FR may also alter the partitioning of photosynthetic assimilates between organs. Findings in the regulation of dry mass partitioning in plants were summarized and they demonstrated a knowledge gap between a well-studied regulatory network downstream the perception of FR and a set of FR-induced growth responses. Lastly, the research of this thesis was introduced and the different approaches for each of the research questions were outlined.

Chapter 2 demonstrated the genotypic variation within 33 different tomato genotypes in their responses to FR at the young plant stage. Genotypes responded similarly in plant height, stem dry mass, and shoot: root ratio, i.e., they all increased with increasing FR. However, the response of total plant dry mass varied among genotypes. Then, genotypes were categorized into three groups (a strong, moderate, and weak responding group) based on their relative response in total plant dry mass to FR. Growth component analysis revealed that tomato genotypes that increased strongly in growth response to FR, compared to the moderate and weak responding ones, were characterized by a strong increase in net assimilation rate.

Chapter 3 continued from the finding in the previous chapter that young plants of all genotypes increased in their shoot: root ratio with FR. Using both wild type and loss-of-function double mutant of phyB1/B2, it was demonstrated that the FR-induced increase in shoot: root ratio involved phytochrome B, as the phyB1/B2 double mutant also showed a strong increase in shoot: root ratio when grown without FR. Interestingly, the phyB1/B2 double mutant still responded in shoot: root ratio when FR increased, providing evidence for the involvement of other phytochromes in the regulation of shoot: root ratio in tomato. Lastly, it was demonstrated that the phytochrome-regulated response of shoot: root ratio to FR may be mediated by affecting auxin transport.

Chapter 4 focused on fruit-bearing tomato plants and demonstrated the FR effect on tomato fruit growth, and the main cause for this effect. FR significantly increased total fruit dry mass. Growth component analysis revealed that FR increased tomato fruit production mainly by increasing the fraction of dry mass partitioned to fruits, rather than improving photosynthesis and total plant dry mass. Furthermore, FR also reduced the resistance of tomato leaves against Botrytis cinerea.

Chapter 5 explained how FR increased the fraction of dry mass partitioned to fruits. Sink strength, quantified as the growth rate of an organ under non-limiting assimilate supply, is the intrinsic capacity of an organ to attract assimilates and the main determinant of dry mass partitioning. FR increased fruit sink strength by 38% in the glasshouse experiment. Based on this measurement, the model simulation showed that such an increase in sink strength resulted in increased dry mass partitioned to fruits, and the simulation result quantitatively agreed very well with experimentally measured partitioning fractions. FR also increased fruit sugar concentration and upregulated the expression of genes associated with both sugar transport and metabolism. Taken together, it was concluded that FR stimulates dry mass partitioning to fruits mainly by increasing fruit sink strength via simultaneous upregulation of sugar transport and metabolism.

Chapter 6 summarized the findings of the experimental chapters and extended the interpretation and discussion of these findings. The promotional effect of FR in tomato growth comes at a cost in the form of reduced resistance against pathogens. However, FR may increase plants’ tolerance against abiotic stress such as salt stress. The understanding of these trade-offs is far from complete. Also, I discussed the potential of targeting FR responses and sink activity in yield improvement. It was demonstrated that there is genotypic variation in tomato’s growth responses to FR, thus providing the foundation for breeding. FR increased fruit growth in tomato by increasing fruit sink strength, and genes responsible for sink strength were extensively studied. Therefore, it was intriguing to attempt to specifically select varieties with higher fruit sink strength. Powerful tools such as CRISPR and speed breeding are expected to further accelerate this breeding process. Furthermore, I discussed the possibility of integrating FR in modern greenhouse production based on the effects of not only yield improvement but also an enhancement in product quality. Finally, I provided perspectives for future research which will not only help complete our understanding of the plant’s response to FR but also assist the application of FR in modern agriculture production.