Increased temperatures caused by global warming threaten agricultural production, as warmer conditions can inhibit plant growth and development or even destroy crops in extreme circumstances. Extensive research over the past several decades has revealed that chloroplasts, the photosynthetic organelles of plants, are highly sensitive to heat stress, which affects a variety of photosynthetic processes including chlorophyll biosynthesis, photochemical reactions, electron transport, and CO2 assimilation. Important mechanisms by which plant cells respond to heat stress to protect these photosynthetic organelles have been identified and analyzed. More recent studies have made it clear that chloroplasts play an important role in inducing the expression of nuclear heat-response genes during the heat stress response. In this review, we summarize these important advances in plant-based research and discuss how the sensitivity, responses, and signaling roles of chloroplasts contribute to plant heat sensitivity and tolerance.

Sensitivity and Responses of Chloroplasts to Heat Stress in Plants.

Crop production is facing unprecedented challenges. Despite the fact that the food supply has significantly increased over the past half-century, ~8.9 and 14.3% people are still suffering from hunger and malnutrition, respectively. Agricultural environments are continuously threatened by a booming world population, a shortage of arable land, and rapid changes in climate. To ensure food and ecosystem security, there is a need to design future crops for sustainable agriculture development by maximizing net production and minimalizing undesirable effects on the environment. The future crops design projects, recently launched by the National Natural Science Foundation of China and Chinese Academy of Sciences (CAS), aim to develop a roadmap for rapid design of customized future crops using cutting-edge technologies in the Breeding 4.0 era. In this perspective, we first introduce the background and missions of these projects. We then outline strategies to design future crops, such as improvement of current well-cultivated crops, de novo domestication of wild species and redomestication of current cultivated crops. We further discuss how these ambitious goals can be achieved by the recent development of new integrative omics tools, advanced genome-editing tools and synthetic biology approaches. Finally, we summarize related opportunities and challenges in these projects.

Designing future crops: challenges and strategies for sustainable agriculture.

The spermatophyte root system is composed of a primary root that develops from an embryonically formed root meristem, and of different post-embryonic root types: lateral and adventitious roots. Adventitious roots, arising from the stem of the plants, are the main component of the mature root system of many plants. Their development can also be induced in response to adverse environmental conditions or stresses. Here, in this review, we report on the morphological and functional diversity of adventitious roots and their origin. The hormonal and molecular regulation of the constitutive and inducible adventitious root initiation and development is discussed. Recent data confirmed the crucial role of the auxin/cytokinin balance in adventitious rooting. Nevertheless, other hormones must be considered. At the genetic level, adventitious root formation integrates the transduction of external signals, as well as a core auxin-regulated developmental pathway that is shared with lateral root formation. The knowledge acquired from adventitious root development opens new perspectives to improve micropropagation by cutting in recalcitrant species, root system architecture of crops such as cereals, and to understand how plants adapted during evolution to the terrestrial environment by producing different post-embryonic root types.

https://www.mdpi.com/2223-7747/8/7/240/pdf

What Makes Adventitious Roots

High temperature is an abiotic stress factor that threatens plant growth and development. Autophagy in response to heat stress involves the selective removal of heat-induced protein complexes. Previously, we showed that a crucial autophagy protein from apple, MdATG18a, has a positive effect on drought tolerance. In the present study, we treated transgenic apple (Malus domestica) plants overexpressing MdATG18a with high temperature and found that autophagy protected them from heat stress. Overexpression of MdATG18a in apple enhanced antioxidase activity and contributed to the production of increased beneficial antioxidants under heat stress. Transgenic apple plants exhibited higher photosynthetic capacity, as shown by the rate of CO2 assimilation, the maximum photochemical efficiency of photosystem II (PSII), the effective quantum yield, and the electron transport rates in photosystems I and II (PSI and PSII, respectively). We also detected elevated autophagic activity and reduced damage to chloroplasts in transgenic plants compared to WT plants. In addition, the transcriptional activities of several HSP genes were increased in transgenic apple plants. In summary, we propose that autophagy plays a critical role in basal thermotolerance in apple, primarily through a combination of enhanced antioxidant activity and reduced chloroplast damage.

/pdf/mdatg18a-overexpression-improves-basal-thermotolerance-in-2of80kiox9.pdf

MdATG18a overexpression improves basal thermotolerance in transgenic apple by decreasing damage to chloroplasts.

The involvement of nitric oxide (NO) and hydrogen sulfide (H2S) in countermanding heat-inhibited photosynthetic features were studied in wheat (Triticum aestivum L.). Heat stress (HS) was employed at 40 °C after establishment for 6 h daily, and then plants were allowed to recover at 25 °C and grown for 30 days. Glucose (Glc) content increased under HS and repressed plant photosynthetic ability, but the application of sodium nitroprusside (SNP, as NO donor) either alone or with sodium hydrosulfide (NaHS, as H2S donor) reduced Glc-mediated photosynthetic suppression by enhancing ascorbate-glutathione (AsA-GSH) metabolism and antioxidant system, which reduced oxidative stress with decreased H2O2 and TBARS content. Oxidative stress reduction or inhibiting Glc repression was maximum with combined SNP and NaHS treatment, which was substantiated by 2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) and hypotaurine (HT), scavengers for NO and H2S, respectively. The scavenge of H2S reduced NO-mediated alleviation of HS suggesting of its downstream action in NO-mediated heat-tolerance. However, a simultaneous decrease of both (NO and H2S) led to higher Glc-mediated repression of photosynthesis and oxidative stress in terms of increased H2O2 content that was comparable to HS plants. Thus, NO and H2S cooperate to enhance photosynthesis under HS by reducing H2O2-induced oxidative stress and excess Glc-mediated photosynthetic suppression.

/pdf/nitric-oxide-and-hydrogen-sulfide-coordinately-reduce-11vcu8yfzn.pdf

Nitric Oxide and Hydrogen Sulfide Coordinately Reduce Glucose Sensitivity and Decrease Oxidative Stress via Ascorbate-Glutathione Cycle in Heat-Stressed Wheat (Triticum aestivum L.) Plants.

Increases in ambient temperatures have been a severe threat to crop production in many countries around the world under climate change. Chloroplasts serve as metabolic centers and play a key role in physiological adaptive processes to heat stress. In addition to expressing heat shock proteins that protect proteins from heat-induced damage, metabolic reprogramming occurs during adaptive physiological processes in chloroplasts. Heat stress leads to inhibition of plant photosynthetic activity by damaging key components functioning in a variety of metabolic processes, with concomitant reductions in biomass production and crop yield. In this review article, we will focus on events through extensive and transient metabolic reprogramming in response to heat stress, which included chlorophyll breakdown, generation of reactive oxygen species (ROS), antioxidant defense, protein turnover, and metabolic alterations with carbon assimilation. Such diverse metabolic reprogramming in chloroplasts is required for systemic acquired acclimation to heat stress in plants.

Metabolic Reprogramming in Chloroplasts under Heat Stress in Plants

In photosynthetic organisms, the photosystem II (PSII) complex is the primary target of thermal damage. Plants have evolved a repair process to prevent the accumulation of damaged PSII. The repair of PSII largely involves de novo synthesis of proteins, particularly the D1 subunit protein encoded by the chloroplast gene psbA. Here we report that the allotropic expression of the psbA complementary DNA driven by a heat-responsive promoter in the nuclear genome sufficiently protects PSII from severe loss of D1 protein and dramatically enhances survival rates of the transgenic plants of Arabidopsis, tobacco and rice under heat stress. Unexpectedly, we found that the nuclear origin supplementation of the D1 protein significantly stimulates transgenic plant growth by enhancing net CO2 assimilation rates with increases in biomass and grain yield. These findings represent a breakthrough in bioengineering plants to achieve efficient photosynthesis and increase crop productivity under normal and heat-stress conditions.

Nuclear-encoded synthesis of the D1 subunit of photosystem II increases photosynthetic efficiency and crop yield.

As a ubiquitous reaction, glucosylation controls the bioactivity of cytokinins in plant growth and development. Here we show that genetic manipulation of zeatin-O-glucosylation regulates the formation of important agronomic traits in rice by manipulating the expression of OscZOG1 gene, encoding a putative zeatin O-glucosyltransferase. We found that OscZOG1 was preferentially expressed in shoot and root meristematic tissues and nascent organs. The growth of lateral roots was stimulated in the overexpression lines, but inhibited in RNA interference lines. In shoots, knockdown of OscZOG1 expression by RNA interference significantly improved tillering, panicle branching, grain number per panicle and seed size, which are important agronomic traits for grain yield. In contrast, constitutive expression of OscZOG1 leads to negative effects on the formation of the grain-yielding traits with a marked increase in the accumulation levels of cis-zeatin O-glucoside (cZOG) in the transgenic rice plants. In this study, our findings demonstrate the feasibility of improving the critical yield-determinant agronomic traits, including tiller number, panicle branches, total grain number per panicle and grain weight by downregulating the expression level of OscZOG1. Our results suggest that modulating the levels of cytokinin glucosylation can function as a fine-tuning switch in regulating the formation of agronomic traits in rice.

Putative zeatin O-glucosyltransferase OscZOG1 regulates root and shoot development and formation of agronomic traits in rice

The Calvin-Benson cycle (CBC) consists of three critical processes, including fixation of CO2 by Rubisco, reduction of 3-phosphoglycerate (3PGA) to triose phosphate (triose-P) with NADPH and ATP generated by the light reactions, and regeneration of ribulose 1,5-bisphosphate (RuBP) from triose-P. The activities of photosynthesis-related proteins, mainly from the CBC, were found more significantly affected and regulated in plants challenged with high temperature stress, including Rubisco, Rubisco activase (RCA) and the enzymes involved in RuBP regeneration, such as sedoheptulose-1,7-bisphosphatase (SBPase). Over the past years, the regulatory mechanism of CBC, especially for redox-regulation, has attracted major interest, because balancing flux at the various enzymatic reactions and maintaining metabolite levels in a range are of critical importance for the optimal operation of CBC under high temperature stress, providing insights into the genetic manipulation of photosynthesis. Here, we summarize recent progress regarding the identification of various layers of regulation point to the key enzymes of CBC for acclimation to environmental temperature changes along with open questions are also discussed. 

Qing-Long Wang

Papers

Metabolic Reprogramming in Chloroplasts under Heat Stress in Plants

Nuclear-encoded synthesis of the D1 subunit of photosystem II increases photosynthetic efficiency and crop yield.

Putative zeatin O-glucosyltransferase OscZOG1 regulates root and shoot development and formation of agronomic traits in rice

Regulation of Calvin–Benson cycle enzymes under high temperature stress

Regulation of Calvin–Benson cycle enzymes under high temperature stress