Systemic Signaling in Propelling Crop Yield: Comparison
View Latest Version
Please note this is a comparison between Version 3 by Beatrix Zheng and Version 2 by Beatrix Zheng.

Food security has become a topic of great concern in many countries. Global food security depends heavily on agriculture that has access to proper resources and best practices to generate higher crop yields. Crops, as with other plants, have a variety of strategies to adapt their growth to external environments and internal needs. In plants, the distal organs are interconnected through the vascular system and intricate hierarchical signaling networks, to communicate and enhance survival within fluctuating environments. Photosynthesis and carbon allocation are fundamental to crop production and agricultural outputs. Despite tremendous progress achieved by analyzing local responses to environmental cues, and bioengineering of critical enzymatic processes, little is known about the regulatory mechanisms underlying carbon assimilation, allocation, and utilization.

  • systemic signal
  • photosynthesis
  • carbon assimilation
  • systemic acquired acclimation
  • stomata movement
  • stomata density
  • photosynthate
  • phloem unloading
  • organ development
  • carbon/nitrogen balance

1. Introduction

With the acute demand for enhancing food production within currently changing agricultural environments, researchers are seeking solutions to maintain crop growth under adverse conditions. During the past century, food production has been increased through fertilizer application and field management, the breeding of elite crops [1][2], genetic engineering of plant genomes, etc. [3]. In diversified agricultural ecosystems, crop productivity is largely dependent on the photosynthetic capacity of source organs (net producer of carbohydrates) and assimilation efficiency of photosynthates in sink tissues/organs (net consumption of imported carbon sources).
Great efforts and considerable progress have been made towards understanding the molecular mechanisms and regulatory events in photosynthesis. For example, facilitated by advanced biophysical technologies, researchers have developed well-resolved crystal structures of light-harvesting systems/complexes from cyanobacteria to higher plants, offering a solid basis for the detailed examination of light reactions that occur during photosynthesis [4][5][6][7]. Another important component that determines the enhancement of crop yield is the capacity and efficiency of plants to assimilate carbon dioxide (CO2) from the atmosphere. Recent breakthroughs were reported in the engineering of C3 plants that increased photosynthetic potential by reducing photorespiratory-associated losses [8][9].
Photosynthetic efficiency is critical to improving crop yield and feeding the growing global population [10]. Indeed, C3 crops (cassava, soybean, rice, etc.) benefit from their advanced photosynthetic efficiency and higher CO2 assimilation rates but may require a simultaneous increase in sink capacity to enhance crop yields. This is because the upregulation of carbon utilization, in harvestable sink tissues/organs, will, in turn, enhance the translocation rate of photoassimilates being delivered from the source to the sink, thereby further driving photosynthesis in the source region. Sink strength, the capacity of plants to utilize carbon in sinks, is often reinforced by bioengineering carbohydrate metabolic pathways in sink tissue/organs [11][12]. For example, invertases play important roles in sugar metabolism, which is vital for sink strength regulation in many systems. Cytosolic expression of yeast invertase can lead to a reduction in starch content in potato tubers; however, when the same enzyme was targeted in the potato apoplast, it resulted in the enlargement of tuber size and enhancement of yield [13]. In addition to the regulation of sucrose cleavage by invertases, sink strength may also be adjusted by the enzyme activities involved in the biosynthesis of storage compounds and compartmentation of sucrose in sink cells [14][15].

2. Systemic Regulation of Carbon Assimilation and Allocation

2.1. Photosynthesis

Selective breeding programs have endowed modern crops with high efficiency in expanding leaf area and the translocation of carbon and nutrients into seeds. However, many energy conversion limitations still limit the overall efficiency of photosynthesis. Crops harvested in temperate and tropical areas can only convert 1% of the annual solar irradiance over the same land area [16]. Light and CO2 are two driving forces for photosynthesis. Plants respond to light intensity, light quality (spectral distribution), and CO2 in their habitat through various physiological and developmental adjustments. Plants’ long-distance signaling, i.e., systemic regulation of distal organs/tissues, has attracted increasing attention in terms of being an important adaptation to environmental changes. Integrative studies have indicated that light- and CO2-dependent, leaf-to-leaf long-distance signals mediate processes that are closely related to photosynthesis, and the underlying mechanisms have provided insight into the optimization of crop yield [17][18][19][20].

2.2. Assimilate Loading and Partitioning

The plant vascular system consists of xylem, phloem, and other integral tissues [21]. Xylem functions as an efficient water and mineral nutrient transport system, from root to shoot, and provides essential mechanical strength for the plant body. In mature phloem, enucleate sieve elements (SEs) are sustained by symplasmically interconnected companion cells (CCs), thereby forming a system of sieve element–companion cell (SE-CC) complexes. These complexes connect to surrounding cells via apoplasmic or symplasmic methods [22]. Further, SEs are arranged end-to-end, giving rise to the structure referred to as sieve tubes, which function as the conduit through which the phloem translocation stream moves to transport photosynthates from the source to sink areas of the plant, as well as in the delivery of information molecules to distal organ/tissue [21][23]. Photosynthates flow between source leaves (net production of photoassimilates), and sink organ/tissues (net consumption of resource) can be characterized by three physiological processes in succession: (1) Photosynthates are loaded into collection phloem in minor veins of source leaves; (2) long-distance delivery of these loaded materials to distal sink organs through transport phloem; and (3) photosynthate (generally sucrose) exits from release phloem into the surrounding tissues for utilization or storage. Great efforts have been made to manipulate metabolic enzymes and transporters that are involved in photosynthate assimilation within the source and/or sink organs’ development, endeavoring to improve agricultural output under fluctuating environments [24][25][26][27]. Increasing evidence has pointed out that source–sink interactions play a critical role in regulating plant growth and reproduction, and hence, crop yield [12][28][29]. Moreover, Ham and Lucas [30] have stated that local environmental inputs, as well as global integrators, can adjust or even override the internal metabolic and developmental needs of plants. Here, the researchers will highlight a few examples to discuss recent studies on the systemic regulation of source allocation by phloem-borne long-distance signals.

3. Concluding Remarks and Future Prospects

The ever-increasing demand for food and the simultaneous deterioration of agricultural environments are exacerbating the need to improve crop yield performance. To address this problem, significant efforts are being made to enhance crop production under adverse growth conditions. Numerous studies have established that enhanced photosynthesis can improve crop yield potential [10]. Many of these breeding efforts have sought to improve aspects such as source organ/tissue capacity, including optimizing light capture by changing leaf morphology or light reaction efficiency [24][31], bypassing photorespiration to enhance carbon assimilation and growth [32], modifying rates of sucrose synthesis and sucrose signaling networks [33][34][35], introducing the C4 metabolic pathway into C3 plants [36], and so forth. These advances were primarily based on work focused on local (organ or cell-type specific) responses. Studies on the roles played by systemic signaling in the regulation of adaptive biological processes to biotic and abiotic stresses are still in their infancy. Recently, advanced genomics technologies led to studies that highlighted the need to further explore the broad spectra of mobile signals and their impact on systemic signaling networks [30][37][38][39][40]. Moreover, several proteomics studies revealed the presence of up to thousands of proteins within the phloem exudate by using optimized sample collection techniques and highly sensitive mass spectrometry technology. These detected peptides and proteins, which are loaded into the sieve tube system, may function as systemic signals that regulate biological processes in distantly located sink tissues/organs [41][42][43][44]. Although significant progress has been made in the researchers' understanding of the components present in phloem exudates, under normal and stressed growth conditions, the challenge remains to explore the role of low-abundance phloem-borne proteins in plant development and stress-response signaling pathways. Further improvements to existing proteomics techniques may aid in the discovery and characterization of such low-abundance proteins [45]. Light capture and carbon assimilation capacity are highly correlated with agricultural productivity. Despite abundant evidence of local signaling networks regulating photosynthesis, studies on long-distance signals, potentially involved in orchestrating crop yield performance, are sorely needed. In this research, the researchers assessed advances made in understanding the mechanisms by which systemic (long-distance) signaling adapts young leaves to fluctuating environmental parameters such as light intensity, CO2 levels, and humidity; they also analyzed three examples of mobile proteins, mediating biological processes in both source and sink regions of the plant, to impart information to distal tissues/organs to facilitate plant resilience to prevailing environments. In Table 1, they also summarize additional systemic signals reported to be involved in carbon assimilation and allocation. Clearly, currently available evidence offers support for the notion that further research, aimed at identifying and characterizing mobile molecular players, in conjunction with cutting-edge gene-editing technology [46], will open doors to further improving crop plants. Various genetic, genomic, and epigenetic technologies could be used to engineer functionally mobile signals for manipulating sugar transport, carbon partitioning, and source and/or sink metabolism to modify carbon utilization within specific tissues, in order to enhance crop yield potential.
Table 1. Systemic regulatory signals involved in carbon assimilation and allocation.
Signal Species Characteristics Reference
Carbon Assimilation
ROS, electrical signal and calcium Arabidopsis Systemic signals transmitted from excess light-exposed leaves, to untreated leaves, initiate SAA and protect the photosynthetic efficiency of young developing leaves. [17][47]
ABA Arabidopsis A root-derived hormone that promotes stomatal closure, controlling gas exchange between mesophyll cells and the external environment. [20][48][49]
PHYB Arabidopsis A non-cell-autonomous PHYB mRNA may function as a light-mediated systemic signal to regulate stomatal development within developing leaves. [50][51]
Auxin, MAPK, brassinosteroid, gibberellin acid Arabidopsis Hormones that may function as systemic signals involved in CO2-dependent stomatal development. [52]
Carbon allocation
SlCyp1 tomato A phloem-borne systemic signal that mediates root development, in response to light intensity perceived by the shoot. [53][54][55][56]
SP6A potato A phloem-mobile tuberigen promotes tuberization under short-day conditions. [57][58]
HY5 Arabidopsis A phloem-mobile transcription factor that mediates in light-promoted root extension and nitrate uptake. [59]
S. tuberosum BEL1-LIKE HOMEODOMAIN PROTEIN 5 (StBEL5) potato Graft-transmissible mRNA transcripts move into the root, under short-day conditions, to enhance tuber production. [60]
trehalose 6-phosphate (T6P) maize A potential regulator of whole-plant resource allocation for crop yield improvement. [61]

References

  1. Lemmon, Z.H.; Reem, N.T.; Dalrymple, J.; Soyk, S.; Swartwood, K.E.; Rodriguez-Leal, D.; Van Eck, J.; Lippman, Z.B. Rapid improvement of domestication traits in an orphan crop by genome editing. Nat. Plants 2018, 4, 766–770.
  2. Pingali, P.L. Green revolution: Impacts, limits, and the path ahead. Proc. Natl. Acad. Sci. USA 2012, 109, 12302–12308.
  3. Zhang, C.; Yang, Z.; Tang, D.; Zhu, Y.; Wang, P.; Li, D.; Zhu, G.; Xiong, X.; Shang, Y.; Li, C.; et al. Genome design of hybrid potato. Cell 2021, 184, 3873–3883.e12.
  4. Qin, X.; Suga, M.; Kuang, T.; Shen, J.R. Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 2015, 348, 989–995.
  5. Suga, M.; Akita, F.; Hirata, K.; Ueno, G.; Murakami, H.; Nakajima, Y.; Shimizu, T.; Yamashita, K.; Yamamoto, M.; Ago, H.; et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 2015, 517, 99–103.
  6. Wang, W.; Yu, L.J.; Xu, C.; Tomizaki, T.; Zhao, S.; Umena, Y.; Chen, X.; Qin, X.; Xin, Y.; Suga, M.; et al. Structural basis for blue-green light harvesting and energy dissipation in diatoms. Science 2019, 363, eaav0365.
  7. Pi, X.; Zhao, S.; Wang, W.; Liu, D.; Xu, C.; Han, G.; Kuang, T.; Sui, S.F.; Shen, J.R. The pigment-protein network of a diatom photosystem II-light-harvesting antenna supercomplex. Science 2019, 365, eaax4406.
  8. South, P.F.; Cavanagh, A.P.; Liu, H.W.; Ort, D.R. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 2019, 363, eaat9077.
  9. Huang, W.; Zhang, L.; Columbus, J.T.; Hu, Y.; Zhao, Y.; Tang, L.; Guo, Z.; Chen, W.; McKain, M.; Bartlett, M.; et al. A well-supported nuclear phylogeny of Poaceae and implications for the evolution of C4 photosynthesis. Mol. Plant 2022, 15, 755–777.
  10. Long, S.P.; Marshall-Colon, A.; Zhu, X.G. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 2015, 161, 56–66.
  11. Bihmidine, S.; Hunter, C.T., 3rd; Johns, C.E.; Koch, K.E.; Braun, D.M. Regulation of assimilate import into sink organs: Update on molecular drivers of sink strength. Front. Plant Sci. 2013, 4, 177.
  12. Braun, D.M. Phloem Loading and Unloading of Sucrose: What a Long, Strange Trip from Source to Sink. Annu. Rev. Plant Biol. 2022, 73, 553–584.
  13. Ferreira, S.J.; Sonnewald, U. The mode of sucrose degradation in potato tubers determines the fate of assimilate utilization. Front. Plant Sci. 2012, 3, 23.
  14. Jung, B.; Ludewig, F.; Schulz, A.; Meissner, G.; Wostefeld, N.; Flugge, U.I.; Pommerrenig, B.; Wirsching, P.; Sauer, N.; Koch, W.; et al. Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nat. Plants 2015, 1, 14001.
  15. Nagele, T.; Heyer, A.G. Approximating subcellular organisation of carbohydrate metabolism during cold acclimation in different natural accessions of Arabidopsis thaliana. New Phytol. 2013, 198, 777–787.
  16. Zhu, X.G.; Long, S.P.; Ort, D.R. Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 2010, 61, 235–261.
  17. Karpinski, S.; Reynolds, H.; Karpinska, B.; Wingsle, G.; Creissen, G.; Mullineaux, P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 1999, 284, 654–657.
  18. Zandalinas, S.I.; Fichman, Y.; Devireddy, A.R.; Sengupta, S.; Azad, R.K.; Mittler, R. Systemic signaling during abiotic stress combination in plants. Proc. Natl. Acad. Sci. USA 2020, 117, 13810–13820.
  19. Zhang, J.; De-Oliveira-Ceciliato, P.; Takahashi, Y.; Schulze, S.; Dubeaux, G.; Hauser, F.; Azoulay-Shemer, T.; Toldsepp, K.; Kollist, H.; Rappel, W.J.; et al. Insights into the Molecular Mechanisms of CO2-Mediated Regulation of Stomatal Movements. Curr. Biol. 2018, 28, R1356–R1363.
  20. Kim, T.H.; Bohmer, M.; Hu, H.; Nishimura, N.; Schroeder, J.I. Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 2010, 61, 561–591.
  21. Lucas, W.J.; Groover, A.; Lichtenberger, R.; Furuta, K.; Yadav, S.R.; Helariutta, Y.; He, X.Q.; Fukuda, H.; Kang, J.; Brady, S.M.; et al. The plant vascular system: Evolution, development and functions. J. Integr. Plant Biol. 2013, 55, 294–388.
  22. Lucas, W.J.; Liu, C.M. The plant vascular system I: From resource allocation, inter-organ communication and defense, to evolution of the monocot cambium. J. Integr. Plant Biol. 2017, 59, 290–291.
  23. Gaupels, F. Local and Systemic Defence Signalling in Plants; Universitätsbibliothek: Gießen, Germany, 2016.
  24. Sonnewald, U.; Fernie, A.R. Next-generation strategies for understanding and influencing source-sink relations in crop plants. Curr. Opin. Plant Biol. 2018, 43, 63–70.
  25. Bailey-Serres, J.; Parker, J.E.; Ainsworth, E.A.; Oldroyd, G.E.D.; Schroeder, J.I. Genetic strategies for improving crop yields. Nature 2019, 575, 109–118.
  26. Ort, D.R.; Merchant, S.S.; Alric, J.; Barkan, A.; Blankenship, R.E.; Bock, R.; Croce, R.; Hanson, M.R.; Hibberd, J.M.; Long, S.P.; et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. USA 2015, 112, 8529–8536.
  27. Ludewig, F.; Sonnewald, U. Demand for food as driver for plant sink development. J. Plant Physiol. 2016, 203, 110–115.
  28. Jonik, C.; Sonnewald, U.; Hajirezaei, M.R.; Flugge, U.I.; Ludewig, F. Simultaneous boosting of source and sink capacities doubles tuber starch yield of potato plants. Plant Biotechnol. J. 2012, 10, 1088–1098.
  29. Rossi, M.; Bermudez, L.; Carrari, F. Crop yield: Challenges from a metabolic perspective. Curr. Opin. Plant Biol. 2015, 25, 79–89.
  30. Ham, B.K.; Lucas, W.J. The angiosperm phloem sieve tube system: A role in mediating traits important to modern agriculture. J. Exp. Bot. 2014, 65, 1799–1816.
  31. Kromdijk, J.; Glowacka, K.; Leonelli, L.; Gabilly, S.T.; Iwai, M.; Niyogi, K.K.; Long, S.P. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 2016, 354, 857–861.
  32. Betti, M.; Bauwe, H.; Busch, F.A.; Fernie, A.R.; Keech, O.; Levey, M.; Ort, D.R.; Parry, M.A.; Sage, R.; Timm, S.; et al. Manipulating photorespiration to increase plant productivity: Recent advances and perspectives for crop improvement. J. Exp. Bot. 2016, 67, 2977–2988.
  33. Kretzschmar, T.; Pelayo, M.A.; Trijatmiko, K.R.; Gabunada, L.F.; Alam, R.; Jimenez, R.; Mendioro, M.S.; Slamet-Loedin, I.H.; Sreenivasulu, N.; Bailey-Serres, J.; et al. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat. Plants 2015, 1, 15124.
  34. Griffiths, C.A.; Sagar, R.; Geng, Y.; Primavesi, L.F.; Patel, M.K.; Passarelli, M.K.; Gilmore, I.S.; Steven, R.T.; Bunch, J.; Paul, M.J.; et al. Chemical intervention in plant sugar signalling increases yield and resilience. Nature 2016, 540, 574–578.
  35. Baroja-Fernandez, E.; Munoz, F.J.; Montero, M.; Etxeberria, E.; Sesma, M.T.; Ovecka, M.; Bahaji, A.; Ezquer, I.; Li, J.; Prat, S.; et al. Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol. 2009, 50, 1651–1662.
  36. Von Caemmerer, S.; Quick, W.P.; Furbank, R.T. The development of C(4)rice: Current progress and future challenges. Science 2012, 336, 1671–1672.
  37. Zhang, Z.; Zheng, Y.; Ham, B.K.; Zhang, S.; Fei, Z.; Lucas, W.J. Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency. J. Integr. Plant Biol. 2019, 61, 492–508.
  38. Zhang, Z.; Zheng, Y.; Ham, B.K.; Chen, J.; Yoshida, A.; Kochian, L.V.; Fei, Z.; Lucas, W.J. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat. Plants 2016, 2, 16033.
  39. Lewsey, M.G.; Hardcastle, T.J.; Melnyk, C.W.; Molnar, A.; Valli, A.; Urich, M.A.; Nery, J.R.; Baulcombe, D.C.; Ecker, J.R. Mobile small RNAs regulate genome-wide DNA methylation. Proc. Natl. Acad. Sci. USA 2016, 113, E801–E810.
  40. Kim, G.; LeBlanc, M.L.; Wafula, E.K.; de Pamphilis, C.W.; Westwood, J.H. Plant science. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 2014, 345, 808–811.
  41. Rodriguez-Medina, C.; Atkins, C.A.; Mann, A.J.; Jordan, M.E.; Smith, P.M. Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.). BMC Plant Biol. 2011, 11, 36.
  42. Lin, M.K.; Lee, Y.J.; Lough, T.J.; Phinney, B.S.; Lucas, W.J. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol. Cell Proteom. 2009, 8, 343–356.
  43. Giavalisco, P.; Kapitza, K.; Kolasa, A.; Buhtz, A.; Kehr, J. Towards the proteome of Brassica napus phloem sap. Proteomics 2006, 6, 896–909.
  44. Hu, C.; Ham, B.K.; El-Shabrawi, H.M.; Alexander, D.; Zhang, D.; Ryals, J.; Lucas, W.J. Proteomics and metabolomics analyses reveal the cucurbit sieve tube system as a complex metabolic space. Plant J. 2016, 87, 442–454.
  45. Brinkerhoff, H.; Kang, A.S.W.; Liu, J.; Aksimentiev, A.; Dekker, C. Multiple rereads of single proteins at single-amino acid resolution using nanopores. Science 2021, 374, 1509–1513.
  46. El-Mounadi, K.; Morales-Floriano, M.L.; Garcia-Ruiz, H. Principles, Applications, and Biosafety of Plant Genome Editing Using CRISPR-Cas9. Front. Plant Sci. 2020, 11, 56.
  47. Rossel, J.B.; Wilson, P.B.; Hussain, D.; Woo, N.S.; Gordon, M.J.; Mewett, O.P.; Howell, K.A.; Whelan, J.; Kazan, K.; Pogson, B.J. Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 2007, 19, 4091–4110.
  48. Wang, P.; Song, C.P. Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol. 2008, 178, 703–718.
  49. Acharya, B.R.; Assmann, S.M. Hormone interactions in stomatal function. Plant Mol. Biol. 2009, 69, 451–462.
  50. Devireddy, A.R.; Liscum, E.; Mittler, R. Phytochrome B is Required for Systemic Stomatal Responses and Reactive Oxygen Species Signaling during Light Stress. Plant Physiol. 2020, 184, 1563–1572.
  51. Casson, S.A.; Hetherington, A.M. phytochrome B Is required for light-mediated systemic control of stomatal development. Curr. Biol. 2014, 24, 1216–1221.
  52. Coupe, S.A.; Palmer, B.G.; Lake, J.A.; Overy, S.A.; Oxborough, K.; Woodward, F.I.; Gray, J.E.; Quick, W.P. Systemic signalling of environmental cues in Arabidopsis leaves. J. Exp. Bot. 2006, 57, 329–341.
  53. Ivanchenko, M.G.; Zhu, J.; Wang, B.; Medvecka, E.; Du, Y.; Azzarello, E.; Mancuso, S.; Megraw, M.; Filichkin, S.; Dubrovsky, J.G.; et al. The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation. Development 2015, 142, 712–721.
  54. Spiegelman, Z.; Ham, B.K.; Zhang, Z.; Toal, T.W.; Brady, S.M.; Zheng, Y.; Fei, Z.; Lucas, W.J.; Wolf, S. A tomato phloem-mobile protein regulates the shoot-to-root ratio by mediating the auxin response in distant organs. Plant J. 2015, 83, 853–863.
  55. Zobel, R.W. Some Physiological Characteristics of the Ethylene-requiring Tomato Mutant Diageotropica. Plant Physiol. 1973, 52, 385–389.
  56. Spiegelman, Z.; Omer, S.; Mansfeld, B.N.; Wolf, S. Function of Cyclophilin1 as a long-distance signal molecule in the phloem of tomato plants. J. Exp. Bot. 2017, 68, 953–964.
  57. Navarro, C.; Abelenda, J.A.; Cruz-Oro, E.; Cuellar, C.A.; Tamaki, S.; Silva, J.; Shimamoto, K.; Prat, S. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 2011, 478, 119–122.
  58. Abelenda, J.A.; Bergonzi, S.; Oortwijn, M.; Sonnewald, S.; Du, M.; Visser, R.G.F.; Sonnewald, U.; Bachem, C.W.B. Source-Sink Regulation Is Mediated by Interaction of an FT Homolog with a SWEET Protein in Potato. Curr. Biol. 2019, 29, 1178–1186.e6.
  59. Chen, X.; Yao, Q.; Gao, X.; Jiang, C.; Harberd, N.P.; Fu, X. Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition. Curr. Biol. 2016, 26, 640–646.
  60. Banerjee, A.K.; Chatterjee, M.; Yu, Y.; Suh, S.G.; Miller, W.A.; Hannapel, D.J. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 2006, 18, 3443–3457.
  61. Oszvald, M.; Primavesi, L.F.; Griffiths, C.A.; Cohn, J.; Basu, S.S.; Nuccio, M.L.; Paul, M.J. Trehalose 6-Phosphate Regulates Photosynthesis and Assimilate Partitioning in Reproductive Tissue. Plant Physiol. 2018, 176, 2623–2638.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback