Systemic Signaling: A Role in Propelling Crop Yield

Abstract

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. This review provides insights into vascular-based systemic regulation of photosynthesis and resource allocation, thereby opening the way for the engineering of source and sink activities to optimize the yield performance of major crops.

Keywords: carbon assimilation; carbon/nitrogen balance; organ development; phloem unloading; photosynthate; photosynthesis; stomata density; stomata movement; systemic acquired acclimation; systemic signal.

Figure 1

Systemic acquired acclimation (SAA) occurs through a signal network within the plant vasculature. (a) Schematic representation of an exposed leaf that receives excess excitation energy (EEE), and a systemic leaf, located at a sink region. (b) Proposed signal transduction pathways in SAA. (1) Initial burst of cellular ROS triggers the cascade of cell-to-cell ROS waves, i.e., hydrogen dioxide (H₂O₂) is produced by Respiratory Burst Oxidase Homolog D (RBOHD) (indicated by blue ovals) on the bundle sheath cell plasma membrane. (2) RBOHD relays and maintains an auto-propagating ROS wave along with the plant vascular bundle. Signal amplification propagates rapidly in the companion cell (CC)—sieve element (SE) complexes within the phloem, which may involve calcium ions (Ca²⁺) and electrical signals. (3) In distal unexposed leaves (systemic leaf), the auto-propagated ROS wave and phloem-transmitted signals are perceived by mesophyll cells, thereby a local defense system is triggered, and the cells within young leaf tissues are acclimated in preparation for the approaching strong EEE treatment to protect their photosynthetic efficiency. PPC, phloem parenchyma cell.

Figure 2

Schematic representation of long-distance signaling pathways that control stomatal movement/development. (a) Phytochrome B (PHYB), the red-light receptor, may exert a regulatory function on systemic control of stomatal development in the developing leaves. Under strong light conditions, mature leaf-specific expression of the PHYB gives rise to mobile PHYB transcripts that are delivered to unexposed developing leaves, where they are translated into functional protein to regulate downstream genes, e.g., SPCH, thereby relaying environmental cues (light intensity) from the exposed to developing leaves. Under drought stress, root-derived abscisic acid (ABA) acts as systemic signals to promote stomatal closure, to minimize water loss from the plant. The question mark indicates potential underlying mechanism for long-distance movement of PHYB mRNA, which remains to be elucidated. (b) Increase in CO₂ concentration, sensed by source leaves (major photosynthetic sites), triggers a local signaling network, which initiates downstream cascade responses and communicates the changing condition to young developing leaves. The long-distance signaling may adjust the expression profiles of the genes that are involved in auxin, brassinosteroid (BR), gibberellin acid (GA), and MAPK signaling pathways.

Figure 3

Light promotes root growth and nutrient absorption. (a) CYP1 is a phloem mobile protein that regulates shoot-to-root homeostasis. Light intensity determines the expression level of CYP1 in source leaves. Shoot-derived CYP1 protein accumulates in the roots, leading to activation of the auxin responses, thereby enhancing lateral root formation. Phloem-mediated systemic regulation, through this CYP1 pathway, is also involved in xylem development, which is critical for transport of H₂O and mineral nutrients from roots to shoots. (b) Arabidopsis ELONGATED HYPOCOTYL5 (HY5), a key positive regulator of light signaling, is a phloem mobile transcription factor that traffics from shoot to root. In the aboveground tissue, HY5 binds to the promoters of TPS1, SWEET11, and SWEET12 to regulate carbon fixation and phloem-mediated transport of photoassimilates. Mobile HY5, derived from shoots, binds the promoter regions of HY5 and NRT2.1 genes in the root to promote root growth and nitrate uptake. Both shoot-derived CYP1 and HY5 can lead to enhanced root activity to improve shoot growth. These long-distance signaling agents also contribute to balancing the plant’s shoot-to-root ratio. Red darts indicate up-regulation of described responses.

Figure 4

Mobile SP6A mediates StSWEET11 function in potato tuberization. (a) Sucrose is transported from phloem parenchyma cells (PPC) to companion cells (CC) in the source leaves, using the apoplasmic pathway. Sucrose transporters (SUTs) load sucrose into sieve elements (SEs) and CCs to establish a high concentration in the phloem. Sucrose also can move symplasmically from CCs to SEs through plasmodesmata (PD). High levels of sucrose promote SP6A expression in CCs of source leaves; PD-mediated intercellular movement of SP6A allows its long-distance trafficking through the phloem. (b) In the stolon, sucrose moves symplasmically from SEs to CCs where it is then unloaded, via the StSWEET11 permease, into the apoplasm. Sucrose is retrieved from the apoplast of parenchyma cells (PCs) by the SUTs. (c) Under tuberization, shoot-derived SP6A is unloaded into the stolon CCs where it interacts with StSWEET11 permeases to block apoplasmic sucrose transport between CCs and tuber parenchyma cells (TPCs); thereby, sucrose moves symplasmically from CCs to TPCs. The transition of sucrose unloading pathway in TPCs, from apoplasmic to symplasmic, facilitates tuberization process under high availability of sucrose. Red small round circles indicate sucrose molecules.