For two decades, Baum has led an outstanding and creative molecular nematology research program at Iowa State University that has received national and worldwide recognition. Throughout this exemplary career he has made many significant pioneering contributions that have greatly advanced our understanding and knowledge of the molecular signaling between nematodes and their host plants. These studies produced an extensive series of outstanding contributions on the identification, characterization, and functional analyses of effectors produced by sedentary endoparasitic nematodes. Indeed, the discovery that these nematodes produce in their esophageal gland cells a battery of secreted effectors with functions in parasitism has been one of the greatest conceptual advances in nematology over the last two decades. The Baum lab had the leadership role in expressed sequence tag sequencing and informatics to identify the majority of known phytonematode parasitism genes that encode secreted effector proteins. The Baum lab has also paved the way in functional studies of the nematode effectors, the majority of which are predicted to be novel proteins with unknown functions. For example, his lab was the first to demonstrate that nematode effectors that contained nuclear localization signals could be imported into the nuclei of host cells for potential direct regulatory activity within the host nucleus to promote parasitism.
The cyst nematode effector research originally focused on the agriculturally important Heterodera glycines-soybean interaction. However, in order to tap into the wealth of available Arabidopsis genetic resources, Dr. Baum was the first to extend effector research to a model system of Arabidopsis thaliana–Heterodera schachtii since H. glycines does not infect Arabidopsis and H. schachtii has nearly identical parasitism genes as H. glycines. In one key study, the cyst nematode effector 10A07 co-opts the host posttranslational machinery by physically associating with the host interactive plant kinase to mediate its trafficking to the nucleus where it binds to the IAA16 transcription factor to interfere with auxin signaling. Another significant study showed a secreted cellulose binding protein (HsCBP) directly interacted with a host pectin methylesterase (PME3) to aid cyst nematode parasitism. When HsCBP was overexpressed in Arabidopsis the transgenic plants developed longer roots, exhibited enhanced susceptibility to H. schachtii, and had increased PME3 activity in planta. Likewise, overexpressing PME3 in Arabidopsis produced longer roots and exhibited increased susceptibility to H. schachtii, while a pme3 knockout mutant showed opposite phenotypes. In another important study his group showed that the novel effector 10A06 constitutively expressed in Arabidopsis affected plant morphology, increased susceptibility to H. schachtii as well as to other plant pathogens, and provided an apparent disruption of salicylic acid defense signaling. Spermidine Synthase2 (SPDS2), a key enzyme involved in polyamine biosynthesis, was identified as a specific 10A06 interactor. The collective data from this seminal study generated the hypothesis that increased antioxidant protection and interruption of salicyclic acid signaling are key aspects of 10A06 function during nematode infection. In a related study, his lab showed that although 10A06 orthologs from H. schachtii and H. glycines have high-sequence identity (86%), the effector from H. glycines does not work as a functioning effector in the non-host Arabidopsis. This study is critical because it supports the notion that host range determination among Heterodera species involves sequence differences between orthologous effector proteins.
Baum’s team also has made many major contributions in the molecular analyses of the plant side of the model system of A. thaliana–H. schachtii. MicroRNAs (miRNAs) are a major class of small noncoding RNAs with emerging roles in gene expression via silencing at transcriptional and posttranscriptional levels. In a pioneering study with his associate Tarek Hewezi, Baum was the first to show that miRNAs differentially accumulate in Arabidopsis roots during H. schachtii parasitism, presenting the exciting possibility that host cell gene silencing mechanisms play an important role during cyst nematode parasitism. In elegant follow-up studies, they demonstrated that miR396 is differentially expressed in the cyst nematode feeding cell and functions as an important master switch in syncytium formation by targeting host Growth Regulating Factor genes. Genome-wide expression profiling revealed that the miR396-GRF regulatory system can alter the expression of 44% of the more than 7,000 genes reported to change expression in the Arabidopsis syncytium, implicating miR396 as a key regulator for reprogramming of root cells. A related study showed that Arabidopsis miR827, activated in nematode feeding cells, silenced its nitrogen limitation adaptation target gene to mediate plant susceptibility to H. schachtii by suppressing host immune responses. Baum’s team also developed innovative methods that have significantly contributed to nematode effector research, including an mRNA in-situ hybridization technique that confirmed the expression of putative parasitism genes in the nematode esophageal gland cells. More recently, his lab developed a new method to directly isolate whole esophageal gland cells for transcriptomic analyses that will allow for the first time the identification of effector repertoires and their variability from plant nematodes with different modes of parasitism.
In addition his scholarly contributions to molecular nematology, Baum has made significant commitments undergraduate and graduate education as demonstrated through his teaching activities, mentoring numerous graduate students (9) and postdoctoral research associates (19), and the roles he has played in developing award-winning teaching tools in the form of videos and web-based teaching resources in plant pathology and nematology. Several scientists emanating from his program currently hold university faculty, USDA and industry research positions. This represents an effort not only in scholarship but to the continuation of the discipline through mentoring of the next generation of scientists.