Source: PURDUE UNIVERSITY submitted to NRP
REGULATION AND FUNCTION OF PATHOGEN-INDUCED CALLOSE DEPOSITION IN PLANT IMMUNITY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1016058
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2018
Project End Date
Sep 30, 2023
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
PURDUE UNIVERSITY
(N/A)
WEST LAFAYETTE,IN 47907
Performing Department
Botany & Plant Pathology
Non Technical Summary
Worldwide crop losses due to diseases caused by microbial pathogens and other invasive organisms amount to 20 to 40% global agricultural productivity. An effective and economically sound approach is to exploit plants' natural resistance mechanisms to develop plants inherently resistant or tolerant to diseases. To achieve this goal, it is critical to elucidate complex molecular pathways of plant defense responses. Plant cell wall reinforcement has been recognized for many years as an early plant defense mechanism. For example, during plant interactions with filamentous pathogens, there is a rapid deposition of cell wall appositions called papillae at the sites of pathogen attack. Papillae are rich in callose and other compounds including phenolics and ROS. While the role of phenolics and ROS as antimicrobial molecules has been well established, the role of callose in plant defense has been controversial, largely because of the finding that the pmr4 mutants are deficient in pathogen-induced callose deposition but are hyper-activated in SA responses and consequently more resistance to pathogens. On the other hand, our ubac2 and picc mutants are also compromised in pathogen-induced callose deposition and are hyper-susceptible to pathogen infection. Therefore, it is likely that complete deficiency of both basal and pathogen-induced callose deposition can lead to activation of SA responses, possibly as a compensatory mechanism, and consequently enhanced disease resistance and early senescence of plants. However, our ubac2 and picc mutants are normal in the basal levels of callose deposition but compromised in pathogen-induced callose deposition. Therefore, our proposed comparative analysis of the ubac2, picc and pmr4 mutants could address a long-standing issue on the role of pathogen-induced callose deposition in plant disease resistance.Supporting the role of pathogen-induced callose deposition in plant immune responses is the reports that overexpression of PMR4 callose synthase in plants can lead to increased resistance by preventing or inhibiting pathogen penetration. Our results also indicate that overexpression of PMR4 can lead to increased disease resistance. However, we have discovered that a large percentage of transgenic plants overexpressing PMR4 develop cell death in the mature leaves. This finding raises two important issues. First, both deficiency and overproduction of PMR4 can lead to detrimental effects on plant growth and, therefore, the level and activity of PMR4 must be tightly regulated. Understanding the underlying mechanisms of the regulation of PMR4 can lead to a better understanding of the elaborate mechanisms by which plants balance growth and defense. Second, overexpression of PMR4 has been proposed as a means for genetic engineering of plant disease resistance. However, the detrimental phenotypes of the PMR4-overexpressing lines raise a question about the soundness of the strategy. By understanding the molecular basis for the fitness trade-off of increased callose deposition, it may be possible to develop improved methods to exploit plant cell wall reinforcement to prevent or inhibit pathogen infection without significant negative effects on plant growth.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2122499103050%
2062420104050%
Goals / Objectives
Plant are constantly exposed to a wide range of potential pathogens and through evolution have developed a complex set of defense mechanisms. Pathogen-induced callose deposition is one of important plant defense mechanisms that acts to reinforce plant cell wall at the site of pathogen attack. In Arabidopsis, the PMR4 callose synthase is responsible for pathogen-induced callose accumulation. PMR4 is synthesized in the endoplasmic reticulum (ER) of plant cells and transported through the endosomal system to the plasma membrane. Recently, we have discovered that Arabidopsis mutants for two related proteins (UBAC2a and UBAC2b) implicated in ER protein quality control are hyper-susceptible to the bacterial pathogen Pseudomonas syringae and impaired in pathogen-induced callose deposition. Overexpression of PMR4 in the ubac2 mutants can restore pathogen-induced callose deposition and disease resistance. Interestingly, overexpression of PMR4 in wild-type (WT) plants leads to early senescence of transgenic plants. UBAC2 proteins interact with another ER protein called PICC and the picc mutants are also compromised in plant disease resistance. Based on these preliminary results, we hypothesize that UBAC2 and PICC proteins play a critical role in the biogenesis and trafficking of PMR4 to help ensure proper levels of callose deposition upon pathogen attack. The goal of this project is to understand the novel regulation and role of pathogen-induced, PMR4-dependent callose deposition in plants. The project has three objectives:Establish the mechanisms by which plant UBAC2 proteins regulate pathogen-induced callose deposition by examining their roles in determining the biogenesis and trafficking of PMR4.Determine the role of the UBAC2-interacting PICC protein in pathogen-induced callose deposition.Determine the molecular basis for the fitness cost from both the disruption and overexpression of PMR4 through examination of the role of SA and comparative transcript profiling.
Project Methods
Callose deposition by examining their roles in the biogenesis and trafficking of PMR4.PMR4 is synthesized in the ER and then transported through the endosomal trafficking system to the plasma membrane. Proteins synthesized in the ER go through the ER protein quality control system so that only those properly folded proteins will be transported to their destinations. We hypothesize that UBAC2 proteins in the ER are required for the quality control of PMR4. In the absence of UBAC2 in the ubac2 mutants, PMR4 is synthesized in the ER but compromised in quality control and, therefore, is degraded or retained in the ER. To test this hypothesis, we'll generate the PMR4-GFP fusion gene and place it under its native promoter in a plant binary vector. The PMR4-GFP construct will be transformed into both WT and ubac2 double mutant plants. Both the WT and ubac2 mutant plants containing the PMR4-GFP construct will be infected with a pathogen or treated with a pathogen elicitor. We will the use confocal fluorescence microscopy to examine the levels and subcellular localization of the PMR4-GFP signals. In WT, we expect accumulation of PMR4-GFP signals in the plasma membrane in pathogen-infected or elicitor-treated plants. If UBAC2 proteins play a critical role in the biogenesis of PMR4, we expect that in the ubac2 double mutants, there will be reduced levels of PMR4-GFP signals in the plasma membrane and some of these signals may be retained in the ER.Determine the role of the UBAC2-interacting PICC protein in plant immunity.Like ubac2 double mutants, the picc mutants are compromised in pathogen-triggered immunity (PTI). We hypothesize that the susceptible phenotype of the picc mutant is also due to defects in pathogen-induced callose deposition. To test this, we will directly examine the callose deposition of the picc mutants after pathogen infection or pathogen elicitor treatment. If the picc mutants are indeed compromised in callose deposition, we will determine whether this phenotype can be complemented by overexpression of PMR4. In addition, PICC could act upstream or downstream of UBAC2 or act in a coordinate manner with UBAC2 in pathogen-induced callose deposition. We will use genetic and molecular approaches to test these possibilities. For example, if UBAC2 proteins act upstream of PICC by affecting its synthesis or stability, we expect that overexpression of PICC in the ubac2 double mutants will restore the PTI and pathogen-induced callose deposition in the ubac2 mutants. PICC has a long coiled-coil domain that is known for protein-protein interactions. We will use yeast two-hybrid screens to identify PICC-interacting proteins. The role of the PICC-interacting proteins in PTI and pathogen-induced callose deposition will also be analyzed using molecular and genetic approaches.Determine the molecular basis for the fitness cost from both the disruption and overexpression of PMR4 through examination of the role of SA and comparative transcript profiling. Both the pmr4 mutant and PMR4-overexpressing transgenic plants display early leaf senescence. Previous research has shown that pmr4 mutants show hyper-activated SA responses. To test whether the early senescence of transgenic PMR4-overexpressing plants also results from hyper-activated SA responses, we will introduce the PMR4 overexpression construct into the sid2 and npr1 mutants, which are deficient in SA biosynthesis and signaling, respectively. If SA plays a critical role in PMR4-induced senescence, we expect that the transgenic sid2 and npr1 mutant plants will not develop early senescence even if PMR4 is overexpressed. In addition, we will perform comparative transcript profiling of WT, pmr4 mutant and PMR4-overexpressing plants to identify differentially expressed genes and determine the specific molecular, biochemical and cellular processes that are affected due to the absence or overproduction of PMR4 callose synthase. Once those processes that are most altered in the mutants and overexpression lines for the PMR4 callose synthase are identified, we will further analyze those genes using genetic and molecular approaches to determine their effects on the growth, development and defense responses of the pmr4 mutant and PMR4-overexpression line.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:Scientists and professionals in the fields of agriculture, biology and biotechnology working at universities, companies and other organizations. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One graduate student and one research scientist received training through the project. How have the results been disseminated to communities of interest?One research paper was published in a scientific journal. A graduate student presented a poster on the project in a scientific meeting at Purdue University. The PI present seminars at two universities. What do you plan to do during the next reporting period to accomplish the goals?We plan to determine the molecular basis for the early senescence of the pmr4 mutants by 1) comparing the transcriptomes of the pmr4 mutant plants with wild-type plants, and 2) isolating and charactering genetic suppressors of the pmr4 mutants that no longer display the early senescence phenotypes.

Impacts
What was accomplished under these goals? Pathogen-induced callose deposition is an important plant defense mechanism that acts to reinforce plant cell wall at the site of pathogen attack. In the model plant Arabidopsis, the PMR4 callose synthase is responsible for pathogen-induced callose accumulation. PMR4 is synthesized in the endoplasmic reticulum (ER) of plant cells and transported through the endosomal system to the plasma membrane. We have recently discovered that two related ER proteins UBAC2a and UBAC2b interacts with another ER protein PICC and play a critical role in pathogen-induced callose deposition and in plant immunity. To understand how the UBAC and PICC proteins control pathogen-induced callose deposition, we have generated mutants for the UBAC and PICC proteins and examined their accumulation of the PMR4 callose synthase using protein western blotting and confocal fluorescence microscopy. These studies revealed that the defects in pathogen-induced callose deposition in the ubac and picc mutants were associated with reduced levels of PMR4 callose synthase. Therefore, the UBAC2 and PICC proteins play a critical role in plant immunity by promoting the biogenesis and trafficking of PMR4 to help ensure increased callose deposition upon pathogen attack. We have previously observed that both the pmr4 mutant and PMR4-overexpressing transgenic plants display early leaf senescence. To determine why overexpression of PMR4 has the same phenotype of the pmr4 mutant in early leaf senescence, we performed quantitative RT-PCR to quantify the transcript levels of PMR4 in the overexpression lines. We have discovered that during the early growth stages (less than 6 weeks old), many of the overexpression lines contained elevated levels of PMR4 transcripts. However, during late stages (more then 6 weeks old), the transcript levels of PMR4 were reduced, even below the levels of un-transgenic lines. These lines concomitantly developed early senescence phenotype. These results suggest that the early senescence phenotype of PMR4-overexpression lines was resulted from co-suppression of PMR4. In support of the possibility, when we overexpressed PMR4 in an RNA silencing rdr6 mutant, there was no early senescence phenotype. Previous research has shown that pmr4 mutants show hyper-activated SA responses. To determine whether hyper-activated SA signaling is responsible for the early senescence phenotype, we crossed a pmr4 mutant with a SA-deficient sid2 mutant and generated the pmr4/sid2 mutant. Importantly, the pmr4/sid2 mutant still displays the early senescence phenotype, indicating that SA is not required for the early senescence phenotype of the pmr4 mutant.

Publications

  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wang, M., Li, X., Luo, S., Fan, B., Zhu, C., Chen, Z. (2020) Coordination and crosstalk between autophagosome and multivesicular body pathways in plant stress responses. Cells, 3;9(1):119. doi: 10.3390/cells9010119.


Progress 10/01/18 to 09/30/19

Outputs
Target Audience:Scientists and professionals in the fields of agriculture, biology and biotechnology working at universities, companies and other organizations. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One graduate student and one research scientist received training through the project. Additional 12 graduate and undergraduate students in a class of Molecular Approaches to Plant biology also received training in plant molecular biology through laboratory exercises developed from the project. How have the results been disseminated to communities of interest?One research paper was published in a scientific journal. A graduate student presented a poster on the project in a scientific meeting at Purdue University. The PI present seminars at two universities. What do you plan to do during the next reporting period to accomplish the goals?We plan to determine the molecular basis for the early senescence of the pmr4 mutants by 1) comparing the transcriptomes of the pmr4 mutant plants with wild-type plants, and 2) isolating and charactering genetic suppressors of the pmr4 mutants that no longer display the early senescence phenotypes.

Impacts
What was accomplished under these goals? Pathogen-induced callose deposition is an important plant defense mechanism that acts to reinforce plant cell wall at the site of pathogen attack. In the model plant Arabidopsis, the PMR4 callose synthase is responsible for pathogen-induced callose accumulation. PMR4 is synthesized in the endoplasmic reticulum (ER) of plant cells and transported through the endosomal system to the plasma membrane. We have recently discovered that two related ER proteins UBAC2a and UBAC2b interacts with another ER protein PICC and play a critical role in pathogen-induced callose deposition and in plant immunity. To understand how the UBAC and PICC proteins control pathogen-induced callose deposition, we have generated mutants for the UBAC and PICC proteins and examined their accumulation of the PMR4 callose synthase using protein western blotting and confocal fluorescence microscopy. These studies revealed that the defects in pathogen-induced callose deposition in the ubac and picc mutants were associated with reduced levels of PMR4 callose synthase. Therefore, the UBAC2 and PICC proteins play a critical role in plant immunity by promoting the biogenesis and trafficking of PMR4 to help ensure increased callose deposition upon pathogen attack.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Wang, Z.,�Li, X.,�Wang, X.,�Liu, N.,�Xu, B.,�Peng, Q.,�Guo, Z.,�Fan, B.,� Zhu, C.,�and Chen, Z. (2019) Arabidopsis ER-localized UBAC2 proteins interact with PAMP-INDUCED COILED-COIL to regulate pathogen-induced callose deposition and plant immunity. Plant Cell.�2019 Jan 3. pii: tpc.00334.2018. doi: 10.1105/tpc.18.00334.