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.
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][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
us a solid basis for the detailed examination of light reactions that occur during photosynthesis
[4,5,6,7][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 (CO
2) from the atmosphere. Recent breakthroughs were reported in the engineering of C
3 plants that increased photosynthetic potential by reducing photorespiratory-associated losses
[8,9][8][9].
Photosynthetic efficiency is critical to improving crop yield and feeding the growing global population
[10]. Indeed, C
3 crops (cassava, soybean, rice, etc.) benefit from their advanced photosynthetic efficiency and higher CO
2 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][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][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
[17][16]. Light and CO
2 are two driving forces for photosynthesis. Plants respond to light intensity, light quality (spectral distribution), and CO
2 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 CO
2-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
[18,19,20,21][17][18][19][20].
2.2. Assimilate Loading and Partitioning
The plant vascular system consists of xylem, phloem, and other integral tissues
[83][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
[84][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
[83,85][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
[86,87,88,89][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
[12,90,91][12][28][29]. Moreover, Ham and Lucas
[78][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,
wthe researche
rs 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
[86,117][24][31], bypassing photorespiration to enhance carbon assimilation and growth
[118][32], modifying rates of sucrose synthesis and sucrose signaling networks
[119[33][34][35],
120,121], introducing the C
4 metabolic pathway into C
3 plants
[122][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
[78,123,124,125,126][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
[97,98,127,128][41][42][43][44]. Although significant progress has been made in
outhe researcher
s' 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
[129][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
ourthis re
view, wesearch, 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, CO
2 levels, and humidity;
wthe
y 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,
wthe
y 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
[130][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.