What are the key mechanisms that alter the morphology of stigmatic papillae in Arabidopsis thaliana?

Pollination is one of the critical processes that determines crop yield and quality. Thus, it is an urgent need to elucidate the mechanisms underlying pollination. Our previous research has revealed a novel phenomenon that pollen attachment to stigma caused stigma shrinkage, whereas failure of pollen attachment to stigma due to the environmental stress induced elongation of stigmatic papillae. However, little is known about the mechanisms of these morphological alterations in stigmatic papillae. Since the RLK-ROPGEF-ROP network is a common mechanism for the elongation of pollen tubes and root hairs, this network may be also involved in the elongation of papillae in the stigma. In this review, we will discuss the known mechanisms regulating pollen tube growth and root hair elongation and attempt to propose an elongation mechanism of stigmatic papillae. In addition, we will suggest that the degradation of F-actin by a significant increase in Ca2+ induced by the components of pollen coat might be a putative molecular mechanism of stigmatic papillae shrinkage during pollen adhesion.

Links between Regulatory Systems of ROS and Carbohydrates in Reproductive Development.

To thrive on the earth, highly sophisticated systems to finely control reproductive development have been evolved in plants. In addition, deciphering the mechanisms underlying the reproductive development has been considered as a main research avenue because it leads to the improvement of the crop yields to fulfill the huge demand of foods for the growing world population. Numerous studies revealed the significance of ROS regulatory systems and carbohydrate transports and metabolisms in the regulation of various processes of reproductive development. However, it is poorly understood how these mechanisms function together in reproductive tissues. In this review, we discuss mode of coordination and integration between ROS regulatory systems and carbohydrate transports and metabolisms underlying reproductive development based on the hitherto findings. We then propose three mechanisms as key players that integrate ROS and carbohydrate regulatory systems. These include ROS-dependent programmed cell death (PCD), mitochondrial and respiratory metabolisms as sources of ROS and energy, and functions of arabinogalactan proteins (AGPs). It is likely that these key mechanisms govern the various signals involved in the sequential events required for proper seed production.

Failure of Pollen Attachment to the Stigma Triggers Elongation of Stigmatic Papillae in Arabidopsis thaliana.

Pollination is one of key determinants of yield production in important crops, such as grains and beans in which seeds are utilized as agricultural products. Thus, to fulfil food demand for growing world population, it is necessary to elucidate the mechanisms that regulate pollination, leading to increase in yield production. In this study, we compared detailed morphological characteristics of reproductive organs in Arabidopsis thaliana grown under control conditions or subjected to heat stress. Shorter length of anthers, filaments, and petals were observed in plants subjected to heat stress compared to those under control conditions. In contrast, heat stress resulted in enlargement of stigma via elongation of stigmatic papillae. Classification of stigmas based on patterns of pollen attachment indicated that pollen attachment to stigma clearly decreased under heat stress. In addition, artificial pollination experiment demonstrated that stigma shrank when pollen attached, but, continued to enlarge in the absence of pollen. Such modulation of stigma size depending on the presence or absence of pollen was observed both under control and heat stressed conditions. Taken together, these results suggest that elongation of stigmatic papillae is associated with failure of pollen attachment to the stigma, rather than heat stress. Furthermore, histochemical staining experiments suggest that Ca2+ derived from pollen together with O2 - might be associated with morphological alteration of stigma depending on the patterns of pollen attachment.

Memory of 5-min heat stress in Arabidopsis thaliana.

An ability of plants memorizing past heat exposure to modulate the expression of stress response transcripts during recovery is essential for efficient acquired thermotolerance. In this study, we demonstrated that expression of heat response transcripts spiked at 30 min or 1 h, but dramatically declined at 3 h during recoveries following exposure to 5-min heat stress in Arabidopsis. In contrast, expression of transcripts up-regulated by 45-min heat stress was sustained for 30 min or 1 h then declined during recovery. These results suggest that heat memory can be differently modulated depending on the duration of heat exposure, and indicate that plants can memorize even 5-min heat stress to regulate acclimatory responses during recovery. Later hypothesis can be supported by the finding that accumulation of heat response proteins was also modulated during recovery following 5-min heat stress. In addition, 5-min heat stress followed by 3 h recovery was efficient to activate acquired thermotolerance of plants, although spike of transcript expression was observed at 1 h during recovery. These results suggest that plants possess the ability to quickly memorize heat stress and reset cellular states during recovery to adapt to subsequent severe heat stress.

Integration between ROS Regulatory Systems and Other Signals in the Regulation of Various Types of Heat Responses in Plants.

Because of their sessile lifestyle, plants cannot escape from heat stress and are forced to alter their cellular state to prevent damage. Plants, therefore, evolved complex mechanisms to adapt to irregular increases in temperature in the natural environment. In addition to the ability to adapt to an abrupt increase in temperature, plants possess strategies to reprogram their cellular state during pre-exposure to sublethal heat stress so that they are able to survive under subsequent severe heat stress. Such an acclimatory response to heat, i.e., acquired thermotolerance, might depend on the maintenance of heat memory and propagation of long-distance signaling. In addition, plants are able to tailor their specific cellular state to adapt to heat stress combined with other abiotic stresses. Many studies revealed significant roles of reactive oxygen species (ROS) regulatory systems in the regulation of these various heat responses in plants. However, the mode of coordination between ROS regulatory systems and other pathways is still largely unknown. In this review, we address how ROS regulatory systems are integrated with other signaling networks to control various types of heat responses in plants. In addition, differences and similarities in heat response signals between different growth stages are also addressed.

Coordination Between ROS Regulatory Systems and Other Pathways Under Heat Stress and Pathogen Attack.

Regulatory systems of reactive oxygen species (ROS) are known to be integrated with other pathways involving Ca2+ signaling, protein kinases, hormones and programmed cell death (PCD) pathways to regulate defense mechanisms in plants. Coordination between ROS regulatory systems and other pathways needs to be flexibly modulated to finely tune the mechanisms underlying responses of different types of tissues to heat stress, biotic stresses and their combinations during different growth stages. Especially, modulation of the delicate balance between ROS-scavenging and producing systems in reproductive tissues could be essential, because ROS-dependent PCD is required for the proper fertilization, despite the necessity of ROS scavenging to prevent the damage on cells under heat stress and biotic stresses. In this review, we will update the recent findings associated with coordination between multiple pathways under heat stress, pathogen attack and their combinations. In addition, possible integrations between different signals function in different tissues via ROS-dependent long-distance signals will be proposed.

Differences between seedlings and flowers in anti-ROS based heat responses of Arabidopsis plants deficient in cyclic nucleotide gated channel 2.

Cyclic nucleotide gated channel 2 (CNGC2) in Arabidopsis has been identified as one of the putative heat sensors which might play a key role in the regulation of heat acclimation. However, it is still not understood how CNGC2 controls heat stress responses during different growth stages. This study aimed to characterize the differences in heat stress responses between seedlings and flowers of Arabidopsis plants deficient in CNGC2. Seedlings of Arabidopsis plants deficient in CNGC2 showed enhanced tolerance to heat stress accompanied by higher accumulation of heat response proteins such as multiprotein bridging factor 1c (MBF1c), ascorbate peroxidases (APXs) and heat shock proteins (HSPs). On the other hand, seed production of these knockout lines was more sensitive to heat stress. In contrast to seedlings, accumulation of MBF1c and APX proteins in flowers of these knockout lines was lower than or almost comparable with that in WT plants under heat stress. In addition, plants deficient in CNGC2 showed dramatically higher accumulation of H2O2 in flowers, but, only slightly higher accumulation in seedlings compared with WT plants. These results suggest that the stage-dependent differences in heat stress response of Arabidopsis regulated by CNGC2 might rely on regulatory mechanisms of APX1-and MBF1c-dependent pathways and H2O2 homeostasis.