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While both annual and perennial plants store nitrogen resources during the growing season, seasonal N cycling is a hallmark of the perennial habit. In Populus the vegetative storage proteins BSP, WIN4 and PNI288 all play a role in N storage during active growth, whereas BSP is the major form of reduced N storage during winter dormancy. In this review we explore cellular and molecular events implicated in seasonal N cycling in Populus, as well as environmental cues that modulate both the phenology of seasonal N cycling, and the efficiency and proficiency of autumn N resorption. We highlight recent advances that have been made using Populus genomics resources to address processes germane to seasonal N cycling. Genetic and genecological studies are enabling us to connect our understanding of seasonal N cycling at molecular and cellular levels with that at ecophysiological levels. With the genomics resources and foundational knowledge that are now in place, Populus researchers are poised to build an integrative understanding of seasonal N cycling that spans from genomes to ecosystems.

Summary Vegetative storage proteins (VSPs) are known to serve as nitrogen reserves in many dicot plants but remain undiscovered in grasses, most widely grown group of crops globally. We identified and characterized a VSP in maize and demonstrated that its overexpression improved drought tolerance. Nitrogen supplementation selectively induced a mesophyll lipoxygenase (ZmLOX6), which was targeted to chloroplasts by a novel N‐terminal transit peptide of 62 amino acids. When ectopically expressed under the control of various tissue‐specific promoters, it accumulated to a fivefold higher level upon expression in the mesophyll cells than the wild‐type plants. Constitutive expression or targeted expression specifically to the bundle sheath cells increased its accumulation by less than twofold. The overexpressed ZmLOX6 was remobilized from the leaves like other major proteins during grain development. Evaluated in the field over locations and years, transgenic hybrids overexpressing ZmLOX6 in the mesophyll cells significantly outyielded nontransgenic sibs under managed drought stress imposed at flowering. Additional storage of nitrogen as a VSP in maize leaves ameliorated the effect of drought on grain yield.

Green stem disorder (GSD) delays leaf and stem senescence even after pods mature in soybean. In this study, the relationship between GSD severity and vegetative storage protein (VSP) dynamics was investigated under different timings and intensities of depodding treatments. Short growth period (Yukihomare, Yu), GSD-susceptible (Tachinagaha, Tc), and GSD-resistant (Touhoku 129, Th) cultivars were grown under repeated depodding treatments from the R3 growth stage by half [R3 (1/2)] or by one-third [R3 (1/3)], under a single-time depodding treatment at the R5 growth stage by half [R5 (single)], and under no depodding (control). Depodding from R3 decreased the pod number and induced GSD for both Yu and Th. However, the pod weight and stem weight per plant were statistically unchanged from those in control, indicating that remaining pods partially served as a surplus source reservoir in Yu and Th. Tc reduced the pod number and pod weight and unchanged the stem weight in depodding treatments from R3 but induced GSD regardless of the treatments. The growth of single-time depodding at R5 was not different from that of control except the growth parameters of Yu. The relative VSP content temporarily increased 14 days after R3 (DAR3) in all the treatments and cultivars. Although the relative VSP content decreased afterward in Yu and Th, that of Tc increased according to the depodding intensity. In the depodding experiments over three years, a negative correlation tended to be found after 28 DAR3 between VSP accumulation and GSD severity in Th but not in Tc, suggesting that the mechanism underlying N metabolism and GSD occurrence was different between cultivars.

Soybean [Glycine max (L.) Merr.] contains two proteins called vegetative storage proteins (VSPs) that function as temporary storage reserves, but are also closely related to plant acid phosphatases of the haloacid dehalogenase (HAD) superfamily. This study examined the biochemical basis for the relatively low catalytic activity previously reported for these VSPs. The specific activity of purified recombinant VSPα on GMP was about 40-fold lower than for a related soybean root nodule acid phosphatase (APase), which had a specific activity of 845 U mg-1 protein. Conversion of Ser106 to Asp increased VSP activity about 20-fold. This Asp residue is present in nodule APase and is a highly conserved nucleophile in the HAD superfamily. Related VSPs from cultivated soybean and from three wild perennial soybeans, as well as a pod storage protein (PSP) from Phaseolus vulgaris L. all lack the catalytic Asp, suggesting they too are catalytically inefficient. Phylogenetic analysis showed the VSPs and PSP are more closely related to each other than to 21 other VSP-like proteins from several plant species, all of which have the nucleophilic Asp. This study suggests that loss of catalytic activity may be a requirement for the VSPs and PSP to function as storage proteins in legumes.

Green stem disorder (GSD), characterized by delayed stem senescence during seed maturation, complicates harvesting in soybean production. Although GSD is associated with a sink - source imbalance, a rapid and precise evaluation of GSD has not been established. In sink-limited soybean plants, vegetative storage protein (VSP) accumulates. In this study, pot and field experiments were conducted to reevaluate the relationship between GSD, sink - source imbalance caused by soil moisture change, and VSP accumulation as a possible indicator of GSD in Kyoto, Japan over two years. Drought treatment for four weeks from R1 (beginning flowering), R3 (beginning pod), or R5 (beginning seed) growth stage in pots using the short growth-period cultivar Yukihomare reduced sink size in both years, but reduced relative sink mass (pod weight/shoot weight) and increased GSD severity only in 2017, suggesting that sink-source imbalance, affected by soil moisture, can induce GSD. Soil moisture change from around R3 or R5 to maturity in fields using trench-filled or unfilled water tended to change GSD severity but not VSP accumulation in the uppermost fully expanded leaves from R5 (2018) or 15 days before R5 (2019) to 28 days after R5. GSD and VSP responses, however, differed between the two contrasting cultivars, Tachinagaha and Touhoku 129, suggesting the potential usability of VSP for GSD evaluation.

The role of the protein phosphorylation mechanism in the mobilization of vegetative storage proteins (VSPs) is totally unknown. Patatin is the major VSP of the potato (Solanum tuberosum L.) tuber that encompasses multiple differentially phosphorylated isoforms. In this study, temporal changes in the phosphorylation status of patatin isoforms and their involvement in patatin mobilization are investigated using phosphoproteomic methods based on targeted two-dimensional electrophoresis (2-DE). High-resolution 2-DE profiles of patatin isoforms were obtained in four sequential tuber life cycle stages of Kennebec cultivar: endodormancy, bud break, sprouting and plant growth. In-gel multiplex identification of phosphorylated isoforms with Pro-Q Diamond phosphoprotein-specific stain revealed an increase in the number of phosphorylated isoforms after the tuber endodormancy stage. In addition, we found that the phosphorylation status of patatin isoforms significantly changed throughout the tuber life cycle (P < 0.05) using the chemical method of protein dephosphorylation with hydrogen fluoride-pyridine (HF-P) coupled to 2-DE. More specifically, patatin phosphorylation increased by 32% from endodormancy to the tuber sprouting stage and subsequently decreased together with patatin degradation. Patatin isoforms were not randomly mobilized because highly phosphorylated Kuras-isoforms were preferably degraded in comparison to less phosphorylated non-Kuras isoforms. These results lead us to conclude that patatin is mobilized by a mechanism dependent on the phosphorylation status of specific isoforms.

Green stem disorder (GSD) is an important agronomical problem in soybean production because it delays leaf and stem senescence and complicates the harvest. However, a rapid and precise diagnosis of GSD has not yet been established. In this study, the effect of depodding on GSD and vegetative storage protein (VSP) accumulation was investigated in GSD-susceptible cultivar 'Tachinagaha (Tc)' and GSD-resistant experimental line 'Touhoku 129 (Th)' under two different (early and late) sowing dates in 2020 and 2021. Intact Tc plants showed relatively severe GSD at early sowing in 2020 and late sowing in 2021, whereas intact Th plants showed little GSD at both sowing dates and in both years. Meanwhile, depodding reproducibly induced GSD and increased stem weight for both Tc and Th. The relative VSP content peaked 14-21 days after R3 (DAR3) in intact plants and increased afterward in depodded plants. The relative VSP content differed at 28 DAR3 between intact and depodded plants, which was earlier than the timing when SPAD (soil plant analysis development) values differed, suggesting that VSP accumulation might be a better indicator of GSD than the SPAD value. The present study will contribute to the development of tools for diagnosing GSD.

Piriformospora indica , an endophytic fungus of Sebacinales, colonizes the roots of a wide range of host plants and provides various benefits to the plants. Cardamom ( Elettaria cardamomum Maton) is an economically valuable spice crop of the tropics. In this work, we describe differentially expressed transcripts responding to P. indica root colonization in small cardamom for elucidation of molecular basis of growth and development. During the study, a wild genotype of cardamom was propagated under in vitro conditions using full strength Murashige and Skoog medium supplemented with 1 mg l −1 BAP (for shoot induction) and basal MS liquid medium (for root induction). Cardamom plantlets were co-cultivated with P. indica . Microscopic observation confirmed the presence of P. indica inside the roots of cardamom plantlets. Growth parameters of control and P. indica colonized plantlets were observed for three months at an interval of 15 days. P. indica colonization resulted in a significant increase in the morpho-physiological traits of the host plant. The growth enhancement was visible after 15 days of co-culture. There was a significant increase ( p  < 0.05) in the number and length of leaves, height of the plant and chlorophyll content in P. indica colonized plants compared to non-colonized control plant. In addition to this, the expression levels of auxin, nitrate reductase, vegetative storage protein and phosphate transporter genes were upregulated by 3.45, 3.26, 1.62 and 1.19 times respectively by the co-cultivation of P. indica in cardamom plantlets.

The kinetic pattern of protein mobilization in roots, stolons and nodules of white clover (Trifolium repens cv. Grasslands Huia) was studied over a regrowth period following complete defoliation. Defoliation led to a significant decrease in soluble protein in stolons and roots during the first days of regrowth as compared with uncut plants. Protein degradation was also observed in nodules of both uncut and defoliated plants. Two of the proteins characterized (15 and 17·3 kDa), which accumulate mainly in perennial tissues, have previously been referred to as Vegetative Storage Proteins (VSPs). Using plants inoculated with either efficient (potentially functional) or inefficient Rhizobium strains, the 15 kDa VSP appeared to be located exclusively in the nodules, and it cross-reacted positively with antibodies raised against soybean leghaemoglobin. Nevertheless, the kinetics of its hydrolysis-accumulation following defoliation clearly supported the view that it may play a role in nitrogen storage. The 17·3 kDa protein was shown to accumulate in response to exposure to low temperature, and exhibited a seasonal pattern of relative accumulation under field conditions. Results are discussed in terms of the putative role that this VSP may play in overwintering of clover.

Powdery mildew species Oidium neolycopersici ( On ) can cause serious yield losses in tomato production worldwide. Besides on tomato, On is able to grow and reproduce on Arabidopsis. In this study we screened a collection of activation-tagged Arabidopsis mutants and identified one mutant, 3221, which displayed resistance to On , and in addition showed a reduced stature and serrated leaves. Additional disease tests demonstrated that the 3221 mutant exhibited resistance to downy mildew ( Hyaloperonospora arabidopsidis) and green peach aphid ( Myzus persicae) , but retained susceptibility to bacterial pathogen Pseudomonas syringae pv tomato DC3000. The resistance trait and morphological alteration were mutually linked in 3221. Identification of the activation tag insertion site and microarray analysis revealed that ATHB13 , a homeodomain-leucine zipper (HD-Zip) transcription factor, was constitutively overexpressed in 3221. Silencing of ATHB13 in 3221 resulted in the loss of both the morphological alteration and resistance, whereas overexpression of the cloned ATHB13 in Col-0 and Col- eds1 - 2 backgrounds resulted in morphological alteration and resistance. Microarray analysis further revealed that overexpression of ATHB13 influenced the expression of a large number of genes. Previously, it was reported that ATHB13 -overexpressing lines conferred tolerance to abiotic stress. Together with our results, it appears that ATHB13 is involved in the crosstalk between abiotic and biotic stress resistance pathways.